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Distributed corpus callosum involvement in amyotrophic lateral sclerosis: a deterministic tractography study using q-ball imaging

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Abstract

Diffusion tensor imaging (DTI) has become a useful tool for investigating early white matter (WM) abnormalities in motor neuron disease. Furthermore, fiber tracking packages that apply multi-tensorial algorithms, such as q-ball imaging (QBI), have been proposed as alternative approaches to overcome DTI limitations in depicting fiber tracts with different orientations within the same voxel. We explored motor and extra-motor WM tract abnormalities in phenotypically heterogeneous amyotrophic lateral sclerosis (ALS) cases aiming to establish a consistent QBI-based WM signature of disease. We performed a whole-brain, QBI tract-based spatial statistics analysis with deterministic tractography of genu, body and splenium of corpus callosum (CC) and corticospinal tracts (CST) in 20 ALS patients (12 classical and 8 lower motor neuron variants) compared to 20 healthy controls. Mean tract length, fiber volume and density, and generalized fractional anisotropy were extracted and related to clinical indices of pyramidal impairment (upper motor neuron score), disease disability (ALS functional rating scale-revised) and progression. ALS patients showed significantly decreased fiber density and volume, and increased tract length in all regions of CC and left CST (p < 0.05, corrected). In CC body, pyramidal impairment was inversely correlated to fiber density (p = 0.01), while in CC splenium, clinical disability (p = 0.01) and progression (p = 0.02) were inversely correlated to tract length. Our findings further suggest that QBI tractography might represent a promising approach for investigating structural alterations in neurodegenerative diseases and confirm that callosal involvement is a consistent feature of most ALS variants, significantly related to both pyramidal dysfunction and disease disability.

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Abbreviations

ACE-R:

Addenbrooke’s cognitive examination revised

ALS:

Amyotrophic lateral sclerosis

ALSFRS-R:

ALS functional rating scale-revised

BDNF:

Brain-derived neurotrophic factor

CC:

Corpus callosum

CST:

Corticospinal tract

DTI:

Diffusion tensor imaging

DW-MRI:

Diffusion-weighted-magnetic resonance imaging

FMRIB:

Functional magnetic resonance imaging of the brain

FDT:

FMRIB’s diffusion toolbox

FLIRT:

FMRIB’s linear image registration tool

FrSBe:

Frontal systems behavior

FSL:

FMRIB software library

FUS/TLS:

Fused in sarcoma/translocated in liposarcoma

GFA:

Generalized fractional anisotropy

HARDI:

High-angular-resolution diffusion imaging

IGF 1:

Insulin-like growth factor 1

LMN:

Lower motor neuron

MND:

Motor neuron disease

MNI:

Montreal Neurological Institute

ODF:

Orientation distribution function

PMA:

Progressive muscular atrophy

PLS:

Primary lateral sclerosis

QBI:

Q-ball imaging

SMN1:

Survival motor neuron 1

SOD1:

Superoxide dismutase 1

TARDBP:

Transactive response DNA-binding protein

TBSS:

Tract-based spatial statistics

TCFE:

Threshold-free cluster enhancement

TDP-43:

Transactivating DNA binding protein-43

UMN:

Upper motor neuron

VOI:

Volume of interest

WM:

White matter

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Acknowledgments

We thank Dr. Antonella Paccone for her expert technical support.

Conflicts of interest

None.

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Authors and Affiliations

  1. MRI Research Center SUN-FISM, Second University of Naples, 80138, Naples, Italy

    G. Caiazzo, D. Corbo, F. Trojsi, G. Piccirillo, M. Cirillo, M. R. Monsurrò, F. Esposito & Gioacchino Tedeschi

  2. Department of Medical, Surgical, Neurological, Metabolic and Aging Sciences, Second University of Naples, Piazza Miraglia 2, 80138, Naples, Italy

    G. Caiazzo, F. Trojsi, G. Piccirillo, M. Cirillo, M. R. Monsurrò & Gioacchino Tedeschi

  3. Neurological Institute for Diagnosis and Care “Hermitage Capodimonte”, 80131, Naples, Italy

    D. Corbo & Gioacchino Tedeschi

  4. Department of Medicine and Surgery, University of Salerno, Baronissi, 84081, Salerno, Italy

    F. Esposito

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  1. G. Caiazzo
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  2. D. Corbo
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  3. F. Trojsi
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  4. G. Piccirillo
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  5. M. Cirillo
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  6. M. R. Monsurrò
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  7. F. Esposito
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  8. Gioacchino Tedeschi
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Correspondence to Gioacchino Tedeschi.

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G. Caiazzo and D. Corbo have equally contributed to the manuscript.

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Caiazzo, G., Corbo, D., Trojsi, F. et al. Distributed corpus callosum involvement in amyotrophic lateral sclerosis: a deterministic tractography study using q-ball imaging. J Neurol 261, 27–36 (2014). https://doi.org/10.1007/s00415-013-7144-3

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