Brain perivascular spaces and autism: clinical and pathogenic implications from an innovative volumetric MRI study

Our single-center case-control study aimed to evaluate the unclear glymphatic system alteration in autism spectrum disorder (ASD) through an innovative neuroimaging tool which allows to segment and quantify perivascular spaces in the white matter (WM-PVS) with filtering of non-structured noise and i...

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Published in:Frontiers in neuroscience Vol. 17; p. 1205489
Main Authors: Sotgiu, Maria Alessandra, Lo Jacono, Alessandro, Barisano, Giuseppe, Saderi, Laura, Cavassa, Vanna, Montella, Andrea, Crivelli, Paola, Carta, Alessandra, Sotgiu, Stefano
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Language:English
Published: Switzerland Frontiers Research Foundation 23.06.2023
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Abstract Our single-center case-control study aimed to evaluate the unclear glymphatic system alteration in autism spectrum disorder (ASD) through an innovative neuroimaging tool which allows to segment and quantify perivascular spaces in the white matter (WM-PVS) with filtering of non-structured noise and increase of the contrast-ratio between perivascular spaces and the surrounding parenchyma. Briefly, files of 65 ASD and 71 control patients were studied. We considered: ASD type, diagnosis and severity level and comorbidities (i.e., intellectual disability, attention-deficit hyperactivity disorder, epilepsy, sleep disturbances). We also examined diagnoses other than ASD and their associated comorbidities in the control group. When males and females with ASD are included together, WM-PVS grade and WM-PVS volume do not significantly differ between the ASD group and the control group overall. We found, instead, that WM-PVS volume is significantly associated with male sex: males had higher WM-PVS volume compared to females (p = 0.01). WM-PVS dilation is also non-significantly associated with ASD severity and younger age (< 4 years). In ASD patients, higher WM-PVS volume was related with insomnia whereas no relation was found with epilepsy or IQ. We concluded that WM-PVS dilation can be a neuroimaging feature of male ASD patients, particularly the youngest and most severe ones, which may rely on male-specific risk factors acting early during neurodevelopment, such as a transient excess of extra-axial CSF volume. Our findings can corroborate the well-known strong male epidemiological preponderance of autism worldwide.
AbstractList IntroductionOur single-center case–control study aimed to evaluate the unclear glymphatic system alteration in autism spectrum disorder (ASD) through an innovative neuroimaging tool which allows to segment and quantify perivascular spaces in the white matter (WM-PVS) with filtering of non-structured noise and increase of the contrast-ratio between perivascular spaces and the surrounding parenchyma.MethodsBriefly, files of 65 ASD and 71 control patients were studied. We considered: ASD type, diagnosis and severity level and comorbidities (i.e., intellectual disability, attention-deficit hyperactivity disorder, epilepsy, sleep disturbances). We also examined diagnoses other than ASD and their associated comorbidities in the control group.ResultsWhen males and females with ASD are included together, WM-PVS grade and WM-PVS volume do not significantly differ between the ASD group and the control group overall. We found, instead, that WM-PVS volume is significantly associated with male sex: males had higher WM-PVS volume compared to females (p = 0.01). WM-PVS dilation is also non-significantly associated with ASD severity and younger age (< 4 years). In ASD patients, higher WM-PVS volume was related with insomnia whereas no relation was found with epilepsy or IQ.DiscussionWe concluded that WM-PVS dilation can be a neuroimaging feature of male ASD patients, particularly the youngest and most severe ones, which may rely on male-specific risk factors acting early during neurodevelopment, such as a transient excess of extra-axial CSF volume. Our findings can corroborate the well-known strong male epidemiological preponderance of autism worldwide.
Our single-center case-control study aimed to evaluate the unclear glymphatic system alteration in autism spectrum disorder (ASD) through an innovative neuroimaging tool which allows to segment and quantify perivascular spaces in the white matter (WM-PVS) with filtering of non-structured noise and increase of the contrast-ratio between perivascular spaces and the surrounding parenchyma. Briefly, files of 65 ASD and 71 control patients were studied. We considered: ASD type, diagnosis and severity level and comorbidities (i.e., intellectual disability, attention-deficit hyperactivity disorder, epilepsy, sleep disturbances). We also examined diagnoses other than ASD and their associated comorbidities in the control group. When males and females with ASD are included together, WM-PVS grade and WM-PVS volume do not significantly differ between the ASD group and the control group overall. We found, instead, that WM-PVS volume is significantly associated with male sex: males had higher WM-PVS volume compared to females (p = 0.01). WM-PVS dilation is also non-significantly associated with ASD severity and younger age (< 4 years). In ASD patients, higher WM-PVS volume was related with insomnia whereas no relation was found with epilepsy or IQ. We concluded that WM-PVS dilation can be a neuroimaging feature of male ASD patients, particularly the youngest and most severe ones, which may rely on male-specific risk factors acting early during neurodevelopment, such as a transient excess of extra-axial CSF volume. Our findings can corroborate the well-known strong male epidemiological preponderance of autism worldwide.
Our single-center case-control study aimed to evaluate the unclear glymphatic system alteration in autism spectrum disorder (ASD) through an innovative neuroimaging tool which allows to segment and quantify perivascular spaces in the white matter (WM-PVS) with filtering of non-structured noise and increase of the contrast-ratio between perivascular spaces and the surrounding parenchyma. Briefly, files of 65 ASD and 71 control patients were studied. We considered: ASD type, diagnosis and severity level and comorbidities (i.e., intellectual disability, attention-deficit hyperactivity disorder, epilepsy, sleep disturbances). We also examined diagnoses other than ASD and their associated comorbidities in the control group. We found that WM-PVS volume is significantly associated with male sex: males had higher WM-PVS volume compared to females (p=0.01). WM-PVS dilation is also directly associated with ASD severity and younger age (< 4 years). In ASD patients, higher WM-PVS volume was related with insomnia whereas no relation was found with epilepsy or IQ. We concluded that WM-PVS dilation can be a neuroimaging feature of male ASD patients, particularly the youngest and most severe ones, which may rely on male-specific risk factors acting early during neurodevelopment, such as a transient excess of extra-axial CSF volume. Our findings can corroborate the well-known strong male epidemiological preponderance of autism worldwide.
Our single-center case-control study aimed to evaluate the unclear glymphatic system alteration in autism spectrum disorder (ASD) through an innovative neuroimaging tool which allows to segment and quantify perivascular spaces in the white matter (WM-PVS) with filtering of non-structured noise and increase of the contrast-ratio between perivascular spaces and the surrounding parenchyma.IntroductionOur single-center case-control study aimed to evaluate the unclear glymphatic system alteration in autism spectrum disorder (ASD) through an innovative neuroimaging tool which allows to segment and quantify perivascular spaces in the white matter (WM-PVS) with filtering of non-structured noise and increase of the contrast-ratio between perivascular spaces and the surrounding parenchyma.Briefly, files of 65 ASD and 71 control patients were studied. We considered: ASD type, diagnosis and severity level and comorbidities (i.e., intellectual disability, attention-deficit hyperactivity disorder, epilepsy, sleep disturbances). We also examined diagnoses other than ASD and their associated comorbidities in the control group.MethodsBriefly, files of 65 ASD and 71 control patients were studied. We considered: ASD type, diagnosis and severity level and comorbidities (i.e., intellectual disability, attention-deficit hyperactivity disorder, epilepsy, sleep disturbances). We also examined diagnoses other than ASD and their associated comorbidities in the control group.When males and females with ASD are included together, WM-PVS grade and WM-PVS volume do not significantly differ between the ASD group and the control group overall. We found, instead, that WM-PVS volume is significantly associated with male sex: males had higher WM-PVS volume compared to females (p = 0.01). WM-PVS dilation is also non-significantly associated with ASD severity and younger age (< 4 years). In ASD patients, higher WM-PVS volume was related with insomnia whereas no relation was found with epilepsy or IQ.ResultsWhen males and females with ASD are included together, WM-PVS grade and WM-PVS volume do not significantly differ between the ASD group and the control group overall. We found, instead, that WM-PVS volume is significantly associated with male sex: males had higher WM-PVS volume compared to females (p = 0.01). WM-PVS dilation is also non-significantly associated with ASD severity and younger age (< 4 years). In ASD patients, higher WM-PVS volume was related with insomnia whereas no relation was found with epilepsy or IQ.We concluded that WM-PVS dilation can be a neuroimaging feature of male ASD patients, particularly the youngest and most severe ones, which may rely on male-specific risk factors acting early during neurodevelopment, such as a transient excess of extra-axial CSF volume. Our findings can corroborate the well-known strong male epidemiological preponderance of autism worldwide.DiscussionWe concluded that WM-PVS dilation can be a neuroimaging feature of male ASD patients, particularly the youngest and most severe ones, which may rely on male-specific risk factors acting early during neurodevelopment, such as a transient excess of extra-axial CSF volume. Our findings can corroborate the well-known strong male epidemiological preponderance of autism worldwide.
Author Montella, Andrea
Sotgiu, Stefano
Carta, Alessandra
Barisano, Giuseppe
Cavassa, Vanna
Sotgiu, Maria Alessandra
Saderi, Laura
Crivelli, Paola
Lo Jacono, Alessandro
AuthorAffiliation 4 Clinical Epidemiology and Statistics Unit, Department of Medicine, Surgery and Pharmacy, University of Sassari , Sassari , Italy
1 Department of Biomedical Sciences, University of Sassari , Sassari , Italy
3 Department of Neurosurgery, Stanford University , Stanford, CA , United States
5 Radiology Unit, Department of Medicine, Surgery and Pharmacy, University of Sassari , Sassari , Italy
2 Unit of Child Neuropsychiatry, Department of Medicine, Surgery and Pharmacy, University of Sassari , Sassari , Italy
AuthorAffiliation_xml – name: 1 Department of Biomedical Sciences, University of Sassari , Sassari , Italy
– name: 2 Unit of Child Neuropsychiatry, Department of Medicine, Surgery and Pharmacy, University of Sassari , Sassari , Italy
– name: 4 Clinical Epidemiology and Statistics Unit, Department of Medicine, Surgery and Pharmacy, University of Sassari , Sassari , Italy
– name: 3 Department of Neurosurgery, Stanford University , Stanford, CA , United States
– name: 5 Radiology Unit, Department of Medicine, Surgery and Pharmacy, University of Sassari , Sassari , Italy
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/37425010$$D View this record in MEDLINE/PubMed
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Copyright © 2023 Sotgiu, Lo Jacono, Barisano, Saderi, Cavassa, Montella, Crivelli, Carta and Sotgiu. 2023 Sotgiu, Lo Jacono, Barisano, Saderi, Cavassa, Montella, Crivelli, Carta and Sotgiu
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Keywords perivascular spaces
MRI
glymphatic system
Virchow-Robin spaces
autism
Language English
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Snippet Our single-center case-control study aimed to evaluate the unclear glymphatic system alteration in autism spectrum disorder (ASD) through an innovative...
IntroductionOur single-center case–control study aimed to evaluate the unclear glymphatic system alteration in autism spectrum disorder (ASD) through an...
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StartPage 1205489
SubjectTerms Attention deficit hyperactivity disorder
Autism
Brain research
Cerebrospinal fluid
Children & youth
Cognitive ability
Comorbidity
Epidemiology
Epilepsy
glymphatic system
Hyperactivity
Intellectual disabilities
Interviews
Males
Medical records
Missing data
MRI
Neuroimaging
Neuroscience
Parenchyma
Patients
perivascular spaces
Risk factors
Sleep disorders
Substantia alba
Virchow-Robin spaces
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Title Brain perivascular spaces and autism: clinical and pathogenic implications from an innovative volumetric MRI study
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