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

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Abstract

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

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

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

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

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.

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Fig. 1
Fig. 2

Data availability

The handling of data is regulated by the REC approval of the study and institutional policies. Additional information on MRI settings and analysis pipelines is available from the corresponding author on request.

Abbreviations

ALS:

Amyotrophic lateral sclerosis

ALSFRS-r:

Revised amyotrophic lateral sclerosis functional rating scale

ANCOVA:

Analysis of covariance

C9orf72:

Chromosome 9 open reading frame 72

CC:

Corpus callosum

CST:

Corticospinal tract(s)

DTI:

Diffusion tensor imaging

ECAS:

Edinburgh cognitive and Behavioural ALS Screen

EMG:

Electromyogram

EMM:

Estimated marginal mean

FOV:

Field of view

FrSBe:

Frontal System Behavioural Scale

FSL:

FMRIB Software Library

FSL-FAST:

FMRIB’s Automated Segmentation Tool

FSL-FLIRT:

FMRIB’s Linear Image Registration Tool

FSS:

Fatigue Severity Scale

FWE:

Familywise error

GM:

Grey matter

GPEI:

Global Polio Eradication Initiative

HADS:

Hospital Anxiety and Depression Scale

HC:

Healthy control

HSP:

Hereditary spastic paraplegia

IR-SPGR:

Inversion recovery prepared spoiled gradient recalled echo

IR-TSE:

Inversion recovery turbo spin echo sequence

LEoP:

Late effects of polio

LOSP:

Late-onset sequelae of poliomyelitis

Lt:

Left

LL: :

Lower limb

LMN:

Lower motor neuron

MANCOVA:

Multivariate analysis of covariance

MNI152:

Montreal Neurological Institute 152 standard space

PFS:

Piper Fatigue Scale

PLS:

Primary lateral sclerosis

PPS:

Post-polio syndrome

Rt:

Right

ROI:

Region of interest

SD:

Standard deviation

SE-EPI:

Spin-echo echo planar imaging

SENSE:

Sensitivity encoding

SPIR:

Spectral presaturation with inversion recovery

SSRI:

Selective serotonin reuptake inhibitors

T1W:

T1-weighted imaging

TE:

Echo time

TFCE:

Threshold-free cluster enhancement

TI:

Inversion time

TIV:

Total intracranial volume

TR:

Repetition time

UL:

Upper limb

UMN:

Upper motor neuron

WPV:

Wild poliovirus

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Acknowledgements

We acknowledge all patients with post-polio syndrome and the healthy controls for agreeing to participate in this research study. Without their contribution, this study would not have been possible.

Code availability

Not applicable

Funding

This study was supported by the Health Research Board (HRB EIA-2017-019), the Spastic Paraplegia Foundation, Inc. (SPF), the EU Joint Programme–Neurodegenerative Disease Research (JPND), the Andrew Lydon scholarship and the Irish Institute of Clinical Neuroscience (IICN), the Iris O'Brien Foundation.

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Authors and Affiliations

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

    Stacey Li Hi Shing, Jasmin Lope, Rangariroyashe H. Chipika, Orla Hardiman & Peter Bede

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  1. Stacey Li Hi Shing
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  2. Jasmin Lope
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  3. Rangariroyashe H. Chipika
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  4. Orla Hardiman
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  5. Peter Bede
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Contributions

Conceptualisation of the study, drafting the manuscript: SLHS, PB

Neuroimaging analyses: SLHS, JL, PB

Clinical assessments: SLHS, OH, RC

Revisions of the manuscript for intellectual content: SLHS, JL, RC, OH, PB

Corresponding author

Correspondence to Peter Bede.

Ethics declarations

Ethics approval

The study was approved by the Ethics (Medical Research) Committee—Beaumont Hospital, Dublin, Ireland.

Consent to participate

All participants provided informed consent prior to inclusion.

Consent for publication

Not applicable. No individual data is presented, group-level statistics are reported.

Conflict of interest

The authors declare no competing interests.

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Li Hi Shing, S., Lope, J., Chipika, R.H. et al. Extra-motor manifestations in post-polio syndrome (PPS): fatigue, cognitive symptoms and radiological features. Neurol Sci 42, 4569–4581 (2021). https://doi.org/10.1007/s10072-021-05130-4

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  • DOI: https://doi.org/10.1007/s10072-021-05130-4

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