Extra-motor manifestations in post-polio syndrome (PPS): fatigue, cognitive symptoms and radiological features.


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:
Nov 2021
Historique:
received: 22 12 2020
accepted: 20 02 2021
pubmed: 27 2 2021
medline: 21 10 2021
entrez: 26 2 2021
Statut: ppublish

Résumé

There is a paucity of cerebral neuroimaging studies in post-polio syndrome (PPS), despite the severity of neurological and neuropsychological sequelae associated with the condition. Fatigue, poor concentration, limited exercise tolerance, paraesthesia and progressive weakness are frequently reported, but the radiological underpinnings of these symptoms are poorly characterised. The aim of this study is to evaluate cortical and subcortical alterations in a cohort of adult polio survivors to explore the anatomical substrate of extra-motor manifestations. Thirty-six patients with post-polio syndrome, a disease-control group with amyotrophic lateral sclerosis patients and a cohort of healthy individuals were included in a prospective neuroimaging study with a standardised clinical and radiological protocol. Validated clinical instruments were utilised to assess mood, cognitive and behavioural domains and specific aspects of fatigue. Cortical thickness analyses, subcortical volumetry, brainstem segmentation and region-of-interest (ROI) white matter analyses were undertaken to assess regional grey and white matter alterations. A high proportion of PPS patients exhibited apathy, verbal fluency deficits and reported self-perceived fatigue. On ROI analyses, cortical atrophy was limited to the cingulate gyrus, and the temporal pole and subcortical atrophy were only detected in the left nucleus accumbens. No FA reductions were noted to indicate white matter degeneration in any of the lobes. Despite the high incidence of extra-motor manifestations in PPS, only limited cortical, subcortical and white matter degeneration was identified. Our findings suggest that non-structural causes, such as polypharmacy and poor sleep, may contribute to the complex symptomatology of post-polio syndrome.

Sections du résumé

BACKGROUND BACKGROUND
There is a paucity of cerebral neuroimaging studies in post-polio syndrome (PPS), despite the severity of neurological and neuropsychological sequelae associated with the condition. Fatigue, poor concentration, limited exercise tolerance, paraesthesia and progressive weakness are frequently reported, but the radiological underpinnings of these symptoms are poorly characterised.
OBJECTIVE OBJECTIVE
The aim of this study is to evaluate cortical and subcortical alterations in a cohort of adult polio survivors to explore the anatomical substrate of extra-motor manifestations.
METHODS METHODS
Thirty-six patients with post-polio syndrome, a disease-control group with amyotrophic lateral sclerosis patients and a cohort of healthy individuals were included in a prospective neuroimaging study with a standardised clinical and radiological protocol. Validated clinical instruments were utilised to assess mood, cognitive and behavioural domains and specific aspects of fatigue. Cortical thickness analyses, subcortical volumetry, brainstem segmentation and region-of-interest (ROI) white matter analyses were undertaken to assess regional grey and white matter alterations.
RESULTS RESULTS
A high proportion of PPS patients exhibited apathy, verbal fluency deficits and reported self-perceived fatigue. On ROI analyses, cortical atrophy was limited to the cingulate gyrus, and the temporal pole and subcortical atrophy were only detected in the left nucleus accumbens. No FA reductions were noted to indicate white matter degeneration in any of the lobes.
CONCLUSIONS CONCLUSIONS
Despite the high incidence of extra-motor manifestations in PPS, only limited cortical, subcortical and white matter degeneration was identified. Our findings suggest that non-structural causes, such as polypharmacy and poor sleep, may contribute to the complex symptomatology of post-polio syndrome.

Identifiants

pubmed: 33635429
doi: 10.1007/s10072-021-05130-4
pii: 10.1007/s10072-021-05130-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

4569-4581

Subventions

Organisme : Health Research Board
ID : EIA-2017-019
Pays : Ireland

Informations de copyright

© 2021. Fondazione Società Italiana di Neurologia.

Références

Gawne AC, Halstead LS (1997) Post-polio syndrome: historical perspective, epidemiology and clinical presentation. NeuroRehabilitation 8(2):73–81. https://doi.org/10.3233/NRE-1997-8202
doi: 10.3233/NRE-1997-8202 pubmed: 24525978
Burke T, Pinto-Grau M, Lonergan K, Bede P, O'Sullivan M, Heverin M, Vajda A, McLaughlin RL, Pender N, Hardiman O (2017) A cross-sectional population-based investigation into behavioral change in amyotrophic lateral sclerosis: subphenotypes, staging, cognitive predictors, and survival. Ann Clin Transl Neurol 4(5):305–317. https://doi.org/10.1002/acn3.407
doi: 10.1002/acn3.407 pubmed: 28491898 pmcid: 5420811
Christidi F, Karavasilis E, Rentzos M, Velonakis G, Zouvelou V, Xirou S, Argyropoulos G, Papatriantafyllou I, Pantolewn V, Ferentinos P, Kelekis N, Seimenis I, Evdokimidis I, Bede P (2019) Hippocampal pathology in amyotrophic lateral sclerosis: selective vulnerability of subfields and their associated projections. Neurobiol Aging 84:178–188. https://doi.org/10.1016/j.neurobiolaging.2019.07.019
doi: 10.1016/j.neurobiolaging.2019.07.019 pubmed: 31629116
Murray D, Hardiman O, Meldrum D (2014) Assessment of subjective and motor fatigue in Polio survivors, attending a Postpolio clinic, comparison with healthy controls and an exploration of clinical correlates. Physiother Theory Pract 30(4):229–235. https://doi.org/10.3109/09593985.2013.862890
doi: 10.3109/09593985.2013.862890 pubmed: 24328931
Nollet F, Beelen A, Prins MH, de Visser M, Sargeant AJ, Lankhorst GJ, de Jong BA (1999) Disability and functional assessment in former polio patients with and without postpolio syndrome. Arch Phys Med Rehabil 80(2):136–143
doi: 10.1016/S0003-9993(99)90110-7
Tersteeg IM, Koopman FS, Stolwijk-Swuste JM, Beelen A, Nollet F, Group CS (2011) A 5-year longitudinal study of fatigue in patients with late-onset sequelae of poliomyelitis. Arch Phys Med Rehabil 92(6):899–904. https://doi.org/10.1016/j.apmr.2011.01.005
doi: 10.1016/j.apmr.2011.01.005 pubmed: 21621666
Bruno RL, Zimmerman JR (2000) Word finding difficulty as a post-polio sequelae. Am J Phys Med Rehabil 79(4):343–348
doi: 10.1097/00002060-200007000-00005
Bruno RL, Galski T, DeLuca J (1993) The neuropsychology of post-polio fatigue. Arch Phys Med Rehabil 74(10):1061–1065
doi: 10.1016/0003-9993(93)90062-F
Hazendonk KM, Crowe SF (2000) A neuropsychological study of the postpolio syndrome: support for depression without neuropsychological impairment. Neuropsychiatry Neuropsychol Behav Neurol 13(2):112–118
pubmed: 10780629
Li Hi Shing S, Chipika RH, Finegan E, Murray D, Hardiman O, Bede P (2019) Post-polio Syndrome: More Than Just a Lower Motor Neuron Disease. Front Neurol 10:773. https://doi.org/10.3389/fneur.2019.00773
doi: 10.3389/fneur.2019.00773 pubmed: 31379723 pmcid: 6646725
Berlly MH, Strauser WW, Hall KM (1991) Fatigue in postpolio syndrome. Arch Phys Med Rehabil 72(2):115–118
pubmed: 1991011
Viana CF, Pradella-Hallinan M, Quadros AA, Marin LF, Oliveira AS (2013) Circadian variation of fatigue in both patients with paralytic poliomyelitis and post-polio syndrome. Arq Neuropsiquiatr 71(7):442–445. https://doi.org/10.1590/0004-282X20130059
doi: 10.1590/0004-282X20130059 pubmed: 23857622
Romigi A, Maestri M (2014) Circadian fatigue or unrecognized restless legs syndrome? The post-polio syndrome model. Front Neurol 5:115. https://doi.org/10.3389/fneur.2014.00115
doi: 10.3389/fneur.2014.00115 pubmed: 25071703 pmcid: 4083448
Bruno RL, Cohen JM, Galski T, Frick NM (1994) The neuroanatomy of post-polio fatigue. Arch Phys Med Rehabil 75(5):498–504
pubmed: 8185440
Christidi F, Karavasilis E, Rentzos M, Kelekis N, Evdokimidis I, Bede P (2018) Clinical and Radiological Markers of Extra-Motor Deficits in Amyotrophic Lateral Sclerosis. Front Neurol 9:1005. https://doi.org/10.3389/fneur.2018.01005
doi: 10.3389/fneur.2018.01005 pubmed: 30524366 pmcid: 6262087
Bodian D (1949) Histopathologic basis of clinical findings in poliomyelitis. Am J Med 6(5):563–578
doi: 10.1016/0002-9343(49)90130-8
Finegan E, Chipika RH, Shing SLH, Hardiman O, Bede P (2019) Primary lateral sclerosis: a distinct entity or part of the ALS spectrum? Amyotroph Lateral Scler Frontotemporal Degener 20(3-4):133–145. https://doi.org/10.1080/21678421.2018.1550518
doi: 10.1080/21678421.2018.1550518 pubmed: 30654671
Nasseroleslami B, Dukic S, Broderick M, Mohr K, Schuster C, Gavin B, McLaughlin R, Heverin M, Vajda A, Iyer PM, Pender N, Bede P, Lalor EC, Hardiman O (2019) Characteristic Increases in EEG Connectivity Correlate With Changes of Structural MRI in Amyotrophic Lateral Sclerosis. Cereb Cortex 29(1):27–41. https://doi.org/10.1093/cercor/bhx301
doi: 10.1093/cercor/bhx301 pubmed: 29136131
Bede P, Querin G, Pradat PF (2018) The changing landscape of motor neuron disease imaging: the transition from descriptive studies to precision clinical tools. Curr Opin Neurol 31(4):431–438. https://doi.org/10.1097/wco.0000000000000569
doi: 10.1097/wco.0000000000000569 pubmed: 29750730
Lebouteux MV, Franques J, Guillevin R, Delmont E, Lenglet T, Bede P, Desnuelle C, Pouget J, Pascal-Mousselard H, Pradat PF (2014) Revisiting the spectrum of lower motor neuron diseases with snake eyes appearance on magnetic resonance imaging. Eur J Neurol 21(9):1233–1241. https://doi.org/10.1111/ene.12465
doi: 10.1111/ene.12465 pubmed: 24847978
Choudhary A, Sharma S, Sankhyan N, Gulati S, Kalra V, Banerjee B, Kumar A (2010) Midbrain and spinal cord magnetic resonance imaging (MRI) changes in poliomyelitis. J Child Neurol 25(4):497–499. https://doi.org/10.1177/0883073809340918
doi: 10.1177/0883073809340918 pubmed: 20139405
Trojan DA, Narayanan S, Francis SJ, Caramanos Z, Robinson A, Cardoso M, Arnold DL (2014) Brain volume and fatigue in patients with postpoliomyelitis syndrome. PM R 6(3):215–220. https://doi.org/10.1016/j.pmrj.2013.09.009
doi: 10.1016/j.pmrj.2013.09.009 pubmed: 24060387
Demir CF, Berilgen MS, Mungen B, Bulut S (2012) Do polio survivors have a higher risk of epilepsy? Epilepsy Res 98(1):72–75. https://doi.org/10.1016/j.eplepsyres.2011.08.019
doi: 10.1016/j.eplepsyres.2011.08.019 pubmed: 21996150
Yunusova Y, Plowman EK, Green JR, Barnett C, Bede P (2019) Clinical Measures of Bulbar Dysfunction in ALS. Front Neurol 10:106. https://doi.org/10.3389/fneur.2019.00106
doi: 10.3389/fneur.2019.00106 pubmed: 30837936 pmcid: 6389633
Devos D, Moreau C, Kyheng M, Garcon G, Rolland AS, Blasco H, Gele P, Timothee Lenglet T, Veyrat-Durebex C, Corcia P, Dutheil M, Bede P, Jeromin A, Oeckl P, Otto M, Meninger V, Danel-Brunaud V, Devedjian JC, Duce JA, Pradat PF (2019) A ferroptosis-based panel of prognostic biomarkers for Amyotrophic Lateral Sclerosis. Sci Rep 9(1):2918. https://doi.org/10.1038/s41598-019-39739-5
doi: 10.1038/s41598-019-39739-5 pubmed: 30814647 pmcid: 30814647
Blasco H, Patin F, Descat A, Garcon G, Corcia P, Gele P, Lenglet T, Bede P, Meininger V, Devos D, Gossens JF, Pradat PF (2018) A pharmaco-metabolomics approach in a clinical trial of ALS: Identification of predictive markers of progression. PLoS One 13(6):e0198116. https://doi.org/10.1371/journal.pone.0198116
doi: 10.1371/journal.pone.0198116 pubmed: 29870556 pmcid: 5988280
Schanke AK, Stanghelle JK, Andersson S, Opheim A, Strom V, Solbakk AK (2002) Mild versus severe fatigue in polio survivors: special characteristics. J Rehabil Med 34(3):134–140. https://doi.org/10.1080/165019702753714165
doi: 10.1080/165019702753714165 pubmed: 12395941
Schuster C, Hardiman O, Bede P (2016) Development of an Automated MRI-Based Diagnostic Protocol for Amyotrophic Lateral Sclerosis Using Disease-Specific Pathognomonic Features: A Quantitative Disease-State Classification Study. PLoS One 11(12):e0167331. https://doi.org/10.1371/journal.pone.0167331
doi: 10.1371/journal.pone.0167331 pubmed: 27907080 pmcid: 5132189
Bede P, Iyer PM, Finegan E, Omer T, Hardiman O (2017) Virtual brain biopsies in amyotrophic lateral sclerosis: Diagnostic classification based on in vivo pathological patterns. NeuroImage Clin 15:653–658. https://doi.org/10.1016/j.nicl.2017.06.010
doi: 10.1016/j.nicl.2017.06.010 pubmed: 28664036 pmcid: 5479963
Bruno RL, Creange SJ, Frick NM (1998) Parallels between post-polio fatigue and chronic fatigue syndrome: a common pathophysiology? Am J Med 105(3A):66S–73S
doi: 10.1016/S0002-9343(98)00161-2
Finegan E, Li Hi Shing S, Chipika RH, Doherty MA, Hengeveld JC, Vajda A, Donaghy C, Pender N, McLaughlin RL, Hardiman O, Bede P (2019) Widespread subcortical grey matter degeneration in primary lateral sclerosis: a multimodal imaging study with genetic profiling. NeuroImage Clinl 24:102089. https://doi.org/10.1016/j.nicl.2019.102089
doi: 10.1016/j.nicl.2019.102089
Finegan E, Chipika RH, Li Hi Shing S, Doherty MA, Hengeveld JC, Vajda A, Donaghy C, McLaughlin RL, Pender N, Hardiman O, Bede P (2019) The clinical and radiological profile of primary lateral sclerosis: a population-based study. J Neurol 266(11):2718–2733. https://doi.org/10.1007/s00415-019-09473-z
doi: 10.1007/s00415-019-09473-z pubmed: 31325016
Ahsberg E (2000) Dimensions of fatigue in different working populations. Scand J Psychol 41(3):231–241. https://doi.org/10.1111/1467-9450.00192
doi: 10.1111/1467-9450.00192 pubmed: 11041305
Koopman FS, Brehm MA, Heerkens YF, Nollet F, Beelen A (2014) Measuring fatigue in polio survivors: content comparison and reliability of the fatigue severity scale and the checklist individual strength. J Rehabil Med 46(8):761–767. https://doi.org/10.2340/16501977-1838
doi: 10.2340/16501977-1838 pubmed: 24941350
Hardiman O, Doherty CP, Elamin M, Bede P (2016) Neurodegenerative disorders: a clinical guide. 2016 edn. Springer International Publishing, Springer Cham Heidelberg New York Dordrecht London© Springer International Publishing Switzerland 2016. doi: https://doi.org/10.1007/978-3-319-23309-3
Palotai M, Guttmann CR (2019) Brain anatomical correlates of fatigue in multiple sclerosis. Mult Scler:1352458519876032. doi: https://doi.org/10.1177/1352458519876032
Kluger BM, Zhao Q, Tanner JJ, Schwab NA, Levy SA, Burke SE, Huang H, Ding M, Price C (2019) Structural brain correlates of fatigue in older adults with and without Parkinson’s disease. NeuroImage Clinl 22:101730. https://doi.org/10.1016/j.nicl.2019.101730
doi: 10.1016/j.nicl.2019.101730
von Gontard A, Zerres K, Backes M, Laufersweiler-Plass C, Wendland C, Melchers P, Lehmkuhl G, Rudnik-Schoneborn S (2002) Intelligence and cognitive function in children and adolescents with spinal muscular atrophy. Neuromuscul Disord 12(2):130–136. https://doi.org/10.1016/s0960-8966(01)00274-7
doi: 10.1016/s0960-8966(01)00274-7
Chipika RH, Finegan E, Li Hi Shing S, Hardiman O, Bede P (2019) Tracking a fast-moving disease: longitudinal markers, monitoring, and clinical trial endpoints in ALS. Front Neurol 10:229. https://doi.org/10.3389/fneur.2019.00229
doi: 10.3389/fneur.2019.00229 pubmed: 30941088 pmcid: 6433752
Burke T, Pinto-Grau M, Lonergan K, Elamin M, Bede P, Costello E, Hardiman O, Pender N (2016) Measurement of social cognition in amyotrophic lateral sclerosis: a population based study. PLoS One 11(8):e0160850. https://doi.org/10.1371/journal.pone.0160850
doi: 10.1371/journal.pone.0160850 pubmed: 27556398 pmcid: 4996502

Auteurs

Stacey Li Hi Shing (S)

Computational Neuroimaging Group, Trinity Biomedical Sciences Institute, Trinity College Dublin, Room 5.43, Pearse Street, Dublin 2, Ireland.

Jasmin Lope (J)

Computational Neuroimaging Group, Trinity Biomedical Sciences Institute, Trinity College Dublin, Room 5.43, Pearse Street, Dublin 2, Ireland.

Rangariroyashe H Chipika (RH)

Computational Neuroimaging Group, Trinity Biomedical Sciences Institute, Trinity College Dublin, Room 5.43, Pearse Street, Dublin 2, Ireland.

Orla Hardiman (O)

Computational Neuroimaging Group, Trinity Biomedical Sciences Institute, Trinity College Dublin, Room 5.43, Pearse Street, Dublin 2, Ireland.

Peter Bede (P)

Computational Neuroimaging Group, Trinity Biomedical Sciences Institute, Trinity College Dublin, Room 5.43, Pearse Street, Dublin 2, Ireland. bedep@tcd.ie.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH