Assessment of the glymphatic function in children with attention-deficit/hyperactivity disorder.

Attention deficit hyperactivity disorder Brain perivascular space Diffusion tensor imaging Glymphatic system Magnetic resonance imaging

Journal

European radiology
ISSN: 1432-1084
Titre abrégé: Eur Radiol
Pays: Germany
ID NLM: 9114774

Informations de publication

Date de publication:
06 Sep 2023
Historique:
received: 30 09 2022
accepted: 14 07 2023
revised: 03 07 2023
medline: 7 9 2023
pubmed: 7 9 2023
entrez: 6 9 2023
Statut: aheadofprint

Résumé

Whether the alternation of the glymphatic system exists in neurodevelopmental disease still remains unclear. In this study, we investigated structural and functional changes in the glymphatic system in the treatment-naïve attention-deficit/hyperactivity disorder (ADHD) children by quantitatively measuring the Virchow-Robin spaces (VRS) volume and diffusion tensor image-analysis along the perivascular space (DTI-ALPS). Forty-seven pediatric ADHD patients and 52 age- and gender-matched typically developing (TD) children were recruited in this prospective study. The VRS volume was calculated using a semi-automated approach in axial T2-weighted images. Diffusivities along the x-, y-, and z-axes in the projection, association, and subcortical neural fiber areas were measured. The ALPS index, a ratio that accentuated water diffusion along the perivascular space, was calculated. The Mann-Whitney U test was used to compare the quantitative parameters; Pearson's correlation was used to analyze the correlation with clinical symptoms. The cerebral VRS volume (mean, 15.514 mL vs. 11.702 mL) and the VRS volume ratio in the ADHD group were larger than those in the TD group (all p < 0.001). The diffusivity along the x-axis in association fiber area and ALPS index were significantly smaller in the ADHD group vs. TD group (mean, 1.40 vs.1.59, p < 0.05 after false discovery rate adjustment). Besides, the ALPS index was related to inattention symptoms of ADHD (r =  - 0.323, p < 0.05). Our study suggests that the glymphatic system alternation may participate in the pathogenesis of ADHD, which may be a new research direction for exploring the mechanisms of psycho-behavioral developmental disorders. Moreover, the VRS volume and ALPS index could be used as the metrics for diagnosing ADHD. Considering the potential relevance of the glymphatic system for exploring the mechanisms of attention deficit/hyperactivity, the Virchow-Robin spaces volume and the analysis along the perivascular space index could be used as additional metrics for diagnosing the disorder. • Increased Virchow-Robin space volume and decreased analysis along the perivascular space index were found in the treatment-naïve attention-deficit/hyperactivity disorder children. • The results of this study indicate that the glymphatic system alternation may have a valuable role in the pathogenesis of attention-deficit/hyperactivity disorder. • The analysis along the perivascular space index is correlated with inattention symptoms of attention-deficit/hyperactivity disorder children.

Identifiants

pubmed: 37673963
doi: 10.1007/s00330-023-10220-2
pii: 10.1007/s00330-023-10220-2
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : National Natural Science Foundation of China
ID : 82001439
Organisme : Natural Science Foundation of Guangdong Province
ID : 2022A1515011910

Informations de copyright

© 2023. The Author(s), under exclusive licence to European Society of Radiology.

Références

Thapar A, Cooper M (2016) Attention deficit hyperactivity disorder. Lancet 387:1240–1250
doi: 10.1016/S0140-6736(15)00238-X pubmed: 26386541
Thomas R, Sanders S, Doust J, Beller E, Glasziou P (2015) Prevalence of attention-deficit/hyperactivity disorder: a systematic review and meta-analysis. Pediatrics 135:e994-1001
doi: 10.1542/peds.2014-3482 pubmed: 25733754
Louveau A, Smirnov I, Keyes TJ et al (2015) Structural and functional features of central nervous system lymphatic vessels. Nature 523:337–341
doi: 10.1038/nature14432 pubmed: 26030524 pmcid: 4506234
Rasmussen MK, Mestre H, Nedergaard M (2018) The glymphatic pathway in neurological disorders. Lancet Neurol 17:1016–1024
doi: 10.1016/S1474-4422(18)30318-1 pubmed: 30353860 pmcid: 6261373
Mogensen FL, Delle C, Nedergaard M (2021) The glymphatic system (En) during inflammation. Int J Mol Sci 22:7491
Shen MD (2018) Cerebrospinal fluid and the early brain development of autism. J Neurodev Disord 10:39
doi: 10.1186/s11689-018-9256-7 pubmed: 30541429 pmcid: 6292033
Vilor-Tejedor N, Alemany S, Forns J et al (2019) Assessment of susceptibility risk factors for ADHD in imaging genetic studies. J Atten Disord 23:671–681
doi: 10.1177/1087054716664408 pubmed: 27535943
Gertje EC, van Westen D, Panizo C, Mattsson-Carlgren N, Hansson O (2021) Association of enlarged perivascular spaces and measures of small vessel and Alzheimer disease. Neurology 96:e193–e202
doi: 10.1212/WNL.0000000000011046 pubmed: 33046608
Salimeen MSA, Liu C, Li X et al (2021) Exploring variances of white matter integrity and the glymphatic system in simple febrile seizures and epilepsy. Front Neurol 12:595647
doi: 10.3389/fneur.2021.595647 pubmed: 33967932 pmcid: 8097149
Taoka T, Masutani Y, Kawai H et al (2017) Evaluation of glymphatic system activity with the diffusion MR technique: diffusion tensor image analysis along the perivascular space (DTI-ALPS) in Alzheimer’s disease cases. Jpn J Radiol 35:172–178
doi: 10.1007/s11604-017-0617-z pubmed: 28197821
Chen HL, Chen PC, Lu CH et al (2021) Associations among cognitive functions, plasma DNA, and diffusion tensor image along the perivascular space (DTI-ALPS) in patients with Parkinson’s disease. Oxid Med Cell Longev 2021:4034509
pubmed: 33680283 pmcid: 7904342
Yang G, Deng N, Liu Y, Gu Y, Yao X (2020) Evaluation of glymphatic system using diffusion MR technique in T2DM cases. Front Hum Neurosci 14:300
doi: 10.3389/fnhum.2020.00300 pubmed: 32922272 pmcid: 7456821
Yokota H, Vijayasarathi A, Cekic M et al (2019) Diagnostic performance of glymphatic system evaluation using diffusion tensor imaging in idiopathic normal pressure hydrocephalus and mimickers. Curr Gerontol Geriatr Res 2019:5675014
doi: 10.1155/2019/5675014 pubmed: 31320896 pmcid: 6609364
Wang X, Valdes Hernandez Mdel C, Doubal F et al (2016) Development and initial evaluation of a semi-automatic approach to assess perivascular spaces on conventional magnetic resonance images. J Neurosci Methods 257:34–44
doi: 10.1016/j.jneumeth.2015.09.010 pubmed: 26416614 pmcid: 4666413
Ballerini L, Lovreglio R, Valdes Hernandez MDC et al (2018) Perivascular spaces segmentation in brain MRI using optimal 3D filtering. Sci Rep 8:2132
doi: 10.1038/s41598-018-19781-5 pubmed: 29391404 pmcid: 5794857
Cai K, Tain R, Das S et al (2015) The feasibility of quantitative MRI of perivascular spaces at 7T. J Neurosci Methods 256:151–156
doi: 10.1016/j.jneumeth.2015.09.001 pubmed: 26358620 pmcid: 4651825
Fischl B (2012) FreeSurfer. Neuroimage 62:774-781
Cui Z, Zhong S, Xu P, He Y, Gong G (2013) PANDA: a pipeline toolbox for analyzing brain diffusion images. Front Hum Neurosci 7:42
doi: 10.3389/fnhum.2013.00042 pubmed: 23439846 pmcid: 3578208
Carotenuto A, Cacciaguerra L, Pagani E, Preziosa P, Filippi M, Rocca MA (2022) Glymphatic system impairment in multiple sclerosis: relation with brain damage and disability. Brain 145:2785–2795. https://doi.org/10.1093/brain/awab454
doi: 10.1093/brain/awab454 pubmed: 34919648
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc Ser B (Methodol) 57:289–300
Plog BA, Nedergaard M (2018) The glymphatic system in central nervous system health and disease: past, present, and future. Annu Rev Pathol 13:379–394
doi: 10.1146/annurev-pathol-051217-111018 pubmed: 29195051 pmcid: 5803388
Bae YJ, Choi BS, Kim JM, Choi JH, Cho SJ, Kim JH (2021) Altered glymphatic system in idiopathic normal pressure hydrocephalus. Parkinsonism Relat Disord 82:56–60
doi: 10.1016/j.parkreldis.2020.11.009 pubmed: 33248394
Nedergaard M, Goldman SA (2020) Glymphatic failure as a final common pathway to dementia. Science 370:50–56
doi: 10.1126/science.abb8739 pubmed: 33004510 pmcid: 8186542
Benveniste H, Liu X, Koundal S, Sanggaard S, Lee H, Wardlaw J (2019) The glymphatic system and waste clearance with brain aging: a review. Gerontology 65:106–119
doi: 10.1159/000490349 pubmed: 29996134
Tripp G, Wickens JR (2009) Neurobiology of ADHD. Neuropharmacology 57:579–589
doi: 10.1016/j.neuropharm.2009.07.026 pubmed: 19627998
Jessen NA, Munk AS, Lundgaard I, Nedergaard M (2015) The glymphatic system: a beginner’s guide. Neurochem Res 40:2583–2599
doi: 10.1007/s11064-015-1581-6 pubmed: 25947369 pmcid: 4636982
Wisor JP (2019) Dopamine and wakefulness: pharmacology, genetics, and circuitry. Handb Exp Pharmacol 253:321–335
doi: 10.1007/164_2018_95 pubmed: 29616340
Wynchank D, Bijlenga D, Beekman AT, Kooij JJS, Penninx BW (2017) Adult attention-deficit/hyperactivity disorder (ADHD) and insomnia: an update of the literature. Curr Psychiatry Rep 19:98
doi: 10.1007/s11920-017-0860-0 pubmed: 29086065
Strauss M, Ulke C, Paucke M et al (2018) Brain arousal regulation in adults with attention-deficit/hyperactivity disorder (ADHD). Psychiatry Res 261:102–108
doi: 10.1016/j.psychres.2017.12.043 pubmed: 29291475
Dunn GA, Nigg JT, Sullivan EL (2019) Neuroinflammation as a risk factor for attention deficit hyperactivity disorder. Pharmacol Biochem Behav 182:22–34
doi: 10.1016/j.pbb.2019.05.005 pubmed: 31103523 pmcid: 6855401
Instanes JT, Halmoy A, Engeland A, Haavik J, Furu K, Klungsoyr K (2017) Attention-deficit/hyperactivity disorder in offspring of mothers with inflammatory and immune system diseases. Biol Psychiatry 81:452–459
doi: 10.1016/j.biopsych.2015.11.024 pubmed: 26809250
Zayats T, Athanasiu L, Sonderby I et al (2015) Genome-wide analysis of attention deficit hyperactivity disorder in Norway. PLoS ONE 10:e0122501
doi: 10.1371/journal.pone.0122501 pubmed: 25875332 pmcid: 4395400
Liddelow SA, Guttenplan KA, Clarke LE et al (2017) Neurotoxic reactive astrocytes are induced by activated microglia. Nature 541:481–487
doi: 10.1038/nature21029 pubmed: 28099414 pmcid: 5404890
Rustenhoven J, Drieu A, Mamuladze T et al (2021) Functional characterization of the dural sinuses as a neuroimmune interface. Cell 184(1000–1016):e1027
Naganawa S, Taoka T (2022) The glymphatic system: a review of the challenges in visualizing its structure and function with MR imaging. Magn Reson Med Sci 21:182–194
doi: 10.2463/mrms.rev.2020-0122 pubmed: 33250472

Auteurs

Yingqian Chen (Y)

Department of Radiology, First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Miaomiao Wang (M)

Department of Radiology, First Affiliated Hospital of Xi'an Jiaotong University, Xi'an, China.

Shu Su (S)

Department of Radiology, First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Yan Dai (Y)

Department of Radiology, First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Mengsha Zou (M)

Department of Radiology, First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Liping Lin (L)

Department of Radiology, First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Long Qian (L)

MR Research, GE Healthcare, Beijing, China.

Xianjun Li (X)

Department of Radiology, First Affiliated Hospital of Xi'an Jiaotong University, Xi'an, China.

Hongyu Zhang (H)

Department of Pediatric, First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Meina Liu (M)

Department of Pediatric, First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Jianping Chu (J)

Department of Radiology, First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Jian Yang (J)

Department of Radiology, First Affiliated Hospital of Xi'an Jiaotong University, Xi'an, China. yj1118@xjtu.edu.cn.

Zhiyun Yang (Z)

Department of Radiology, First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China. yzhyun@mail.sysu.edu.cn.

Classifications MeSH