Resting-state functional-MRI in iNPH: can default mode and motor networks changes improve patient selection and outcome? Preliminary report.

CSF dynamics Default-mode network Idiopathic normal pressure hydrocephalus Motor network Resting-state functional-MRI Tap test Ventriculoperitoneal shunt

Journal

Fluids and barriers of the CNS
ISSN: 2045-8118
Titre abrégé: Fluids Barriers CNS
Pays: England
ID NLM: 101553157

Informations de publication

Date de publication:
26 Jan 2023
Historique:
received: 16 09 2022
accepted: 16 01 2023
entrez: 26 1 2023
pubmed: 27 1 2023
medline: 31 1 2023
Statut: epublish

Résumé

Idiopathic normal pressure hydrocephalus (iNPH) is a progressive and partially reversible form of dementia, characterized by impaired interactions between multiple brain regions. Because of the presence of comorbidities and a lack of accurate diagnostic and prognostic biomarkers, only a minority of patients receives disease-specific treatment. Recently, resting-state functional-magnetic resonance imaging (rs-fMRI) has demonstrated functional connectivity alterations in inter-hemispheric, frontal, occipital, default-mode (DMN) and motor network (MN) circuits. Herein, we report our experience in a cohort of iNPH patients that underwent cerebrospinal fluid (CSF) dynamics evaluation and rs-fMRI. The study aimed to identify functional circuits related to iNPH and explore the relationship between DMN and MN recordings and clinical modifications before and after infusion and tap test, trying to understand iNPH pathophysiology and to predict the best responders to ventriculoperitoneal shunt (VPS) implant. We prospectively collected data regarding clinical assessment, neuroradiological findings, lumbar infusion and tap test of thirty-two iNPH patients who underwent VPS implant. Rs-fMRI was performed using MELODIC-ICA both before and after the tap test. Rs-fMRI data of thirty healthy subjects were also recorded. At the baseline, reduced z-DMN and z-MN scores were recorded in the iNPH cohort compared with controls. Higher z-scores were recorded in more impaired patients. Both z-scores significantly improved after the tap test except in subjects with a low resistance to outflow value and without a significant clinical improvement after the test. A statistically significant difference in mean MN connectivity scores for tap test responders and non-responders was demonstrated both before (p = 0.0236) and after the test (p = 0.00137). A statistically significant main effect of the tap test on DMN connectivity after CSF subtraction was recorded (p = 0.038). Our results suggest the presence of a partially reversible plasticity functional mechanism in DMN and MN. Low values compensate for the initial stages of the disease, while higher values of z-DMN were recorded in older patients with a longer duration of symptoms, suggesting an exhausted plasticity compensation. The standardization of this technique could play a role as a non-invasive biomarker in iNPH disease, suggesting the right time for surgery. Trial Registration Prot. IRB 090/2021.

Sections du résumé

BACKGROUND BACKGROUND
Idiopathic normal pressure hydrocephalus (iNPH) is a progressive and partially reversible form of dementia, characterized by impaired interactions between multiple brain regions. Because of the presence of comorbidities and a lack of accurate diagnostic and prognostic biomarkers, only a minority of patients receives disease-specific treatment. Recently, resting-state functional-magnetic resonance imaging (rs-fMRI) has demonstrated functional connectivity alterations in inter-hemispheric, frontal, occipital, default-mode (DMN) and motor network (MN) circuits. Herein, we report our experience in a cohort of iNPH patients that underwent cerebrospinal fluid (CSF) dynamics evaluation and rs-fMRI. The study aimed to identify functional circuits related to iNPH and explore the relationship between DMN and MN recordings and clinical modifications before and after infusion and tap test, trying to understand iNPH pathophysiology and to predict the best responders to ventriculoperitoneal shunt (VPS) implant.
METHODS METHODS
We prospectively collected data regarding clinical assessment, neuroradiological findings, lumbar infusion and tap test of thirty-two iNPH patients who underwent VPS implant. Rs-fMRI was performed using MELODIC-ICA both before and after the tap test. Rs-fMRI data of thirty healthy subjects were also recorded.
RESULTS RESULTS
At the baseline, reduced z-DMN and z-MN scores were recorded in the iNPH cohort compared with controls. Higher z-scores were recorded in more impaired patients. Both z-scores significantly improved after the tap test except in subjects with a low resistance to outflow value and without a significant clinical improvement after the test. A statistically significant difference in mean MN connectivity scores for tap test responders and non-responders was demonstrated both before (p = 0.0236) and after the test (p = 0.00137). A statistically significant main effect of the tap test on DMN connectivity after CSF subtraction was recorded (p = 0.038).
CONCLUSIONS CONCLUSIONS
Our results suggest the presence of a partially reversible plasticity functional mechanism in DMN and MN. Low values compensate for the initial stages of the disease, while higher values of z-DMN were recorded in older patients with a longer duration of symptoms, suggesting an exhausted plasticity compensation. The standardization of this technique could play a role as a non-invasive biomarker in iNPH disease, suggesting the right time for surgery. Trial Registration Prot. IRB 090/2021.

Identifiants

pubmed: 36703181
doi: 10.1186/s12987-023-00407-6
pii: 10.1186/s12987-023-00407-6
pmc: PMC9878781
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

7

Informations de copyright

© 2023. The Author(s).

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Auteurs

Sara Fabbro (S)

Department of Neurosurgery, ASUFC "Santa Maria Della Misericordia", Piazzale Santa Maria Della Misericordia 15, 33100, Udine, Italy.

Daniele Piccolo (D)

Department of Neurosurgery, ASUFC "Santa Maria Della Misericordia", Piazzale Santa Maria Della Misericordia 15, 33100, Udine, Italy.
Department of Clinical, Diagnostic and Pediatric Sciences, University of Pavia, Via Alessandro Brambilla 74, 27100, Pavia, Italy.

Maria Caterina Vescovi (MC)

Department of Neurosurgery, ASUFC "Santa Maria Della Misericordia", Piazzale Santa Maria Della Misericordia 15, 33100, Udine, Italy.

Daniele Bagatto (D)

Department of Neuroradiology, ASUFC "Santa Maria Della Misericordia", Piazzale Santa Maria Della Misericordia 15, 33100, Udine, Italy.

Yan Tereshko (Y)

Department of Neurology, ASUFC "Santa Maria Della Misericordia", Piazzale Santa Maria Della Misericordia 15, 33100, Udine, Italy.

Enrico Belgrado (E)

Department of Neurology, ASUFC "Santa Maria Della Misericordia", Piazzale Santa Maria Della Misericordia 15, 33100, Udine, Italy.

Marta Maieron (M)

Department of Physics, ASUFC "Santa Maria Della Misericordia", Piazzale Santa Maria Della Misericordia 15, 33100, Udine, Italy.

Maria Cristina De Colle (MC)

Department of Neuroradiology, ASUFC "Santa Maria Della Misericordia", Piazzale Santa Maria Della Misericordia 15, 33100, Udine, Italy.

Miran Skrap (M)

Department of Neurosurgery, ASUFC "Santa Maria Della Misericordia", Piazzale Santa Maria Della Misericordia 15, 33100, Udine, Italy.

Francesco Tuniz (F)

Department of Neurosurgery, ASUFC "Santa Maria Della Misericordia", Piazzale Santa Maria Della Misericordia 15, 33100, Udine, Italy. tuniz.francesco@gmail.com.

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