Impaired glymphatic system revealed by DTI-ALPS in cerebral palsy due to periventricular leukomalacia: relation with brain lesion burden and hand dysfunction.
Brain lesion burden
Cerebral palsy
Glymphatic system
Hand dysfunction
Periventricular leukomalacia
Journal
Neuroradiology
ISSN: 1432-1920
Titre abrégé: Neuroradiology
Pays: Germany
ID NLM: 1302751
Informations de publication
Date de publication:
22 Dec 2023
22 Dec 2023
Historique:
received:
12
08
2023
accepted:
14
12
2023
medline:
22
12
2023
pubmed:
22
12
2023
entrez:
22
12
2023
Statut:
aheadofprint
Résumé
Preterm children with cerebral palsy (CP) often have varying hand dysfunction, while the specific brain injury with periventricular leukomalacia (PVL) cannot quite explain its mechanism. We aimed to investigate glymphatic activity using diffusion tensor image analysis along the perivascular space (DTI-ALPS) method and evaluate its association with brain lesion burden and hand dysfunction in children with CP secondary to PVL. We retrospectively enrolled 18 children with bilateral spastic CP due to PVL and 29 age- and sex-matched typically developing controls. The Manual Ability Classification System (MACS) was used to assess severity of hand dysfunction in CP. A mediation model was performed to explore the relationship among the DTI-ALPS index, brain lesion burden, and the MACS level in children with CP. There were significant differences in the DTI-ALPS index between children with CP and their typically developing peers. The DTI-ALPS index of the children with CP was lower than that of the controls (1.448 vs. 1.625, P = 0.003). The mediation analysis showed that the DTI-ALPS index fully mediated the relationship between brain lesion burden and the MACS level (c' = 0.061, P = 0.665), explaining 80% of the effect. This study provides new insights into the neural basis of hand dysfunction in children with CP, demonstrating an important role of glymphatic impairment in such patients. These results suggest that PVL might affect hand function in children with CP by disrupting glymphatic drainage.
Identifiants
pubmed: 38129651
doi: 10.1007/s00234-023-03269-9
pii: 10.1007/s00234-023-03269-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2023. The Author(s).
Références
Bax M, Tydeman C, Flodmark O (2006) Clinical and MRI correlates of cerebral palsy: the European Cerebral Palsy Study. Jama 296(13):1602–1608. https://doi.org/10.1001/jama.296.13.1602
doi: 10.1001/jama.296.13.1602
pubmed: 17018805
Back SA, Rivkees SA (2004) Emerging concepts in periventricular white matter injury. Semin Perinatol 28(6):405–414. https://doi.org/10.1053/j.semperi.2004.10.010
doi: 10.1053/j.semperi.2004.10.010
pubmed: 15693397
Khwaja O, Volpe JJ (2008) Pathogenesis of cerebral white matter injury of prematurity. Arch Dis Child Fetal Neonatal Ed 93(2):F153–F161. https://doi.org/10.1136/adc.2006.108837
doi: 10.1136/adc.2006.108837
pubmed: 18296574
Galinsky R, Lear CA, Dean JM et al (2018) Complex interactions between hypoxia-ischemia and inflammation in preterm brain injury. Dev Med Child Neurol 60(2):126–133. https://doi.org/10.1111/dmcn.13629
doi: 10.1111/dmcn.13629
pubmed: 29194585
Liu XB, Shen Y, Plane JM et al (2013) Vulnerability of premyelinating oligodendrocytes to white-matter damage in neonatal brain injury. Neurosci Bull 29(2):229–238. https://doi.org/10.1007/s12264-013-1311-5
doi: 10.1007/s12264-013-1311-5
pubmed: 23456565
pmcid: 5561874
Pagnozzi AM, Fiori S, Boyd RN et al (2016) Optimization of MRI-based scoring scales of brain injury severity in children with unilateral cerebral palsy. Pediatr Radiol 46(2):270–279. https://doi.org/10.1007/s00247-015-3473-y
doi: 10.1007/s00247-015-3473-y
pubmed: 26554854
Choi JY, Choi YS, Park ES (2017) Language development and brain magnetic resonance imaging characteristics in preschool children with cerebral palsy. J Speech Lang Hear Res 60(5):1330–1338. https://doi.org/10.1044/2016_jslhr-l-16-0281
doi: 10.1044/2016_jslhr-l-16-0281
pubmed: 28492849
Pagnozzi AM, Dowson N, Doecke J et al (2017) Identifying relevant biomarkers of brain injury from structural MRI: validation using automated approaches in children with unilateral cerebral palsy. PLoS One 12(8):e0181605. https://doi.org/10.1371/journal.pone.0181605
doi: 10.1371/journal.pone.0181605
pubmed: 28763455
pmcid: 5538741
Volpe JJ (2009) Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol 8(1):110–124. https://doi.org/10.1016/s1474-4422(08)70294-1
doi: 10.1016/s1474-4422(08)70294-1
pubmed: 19081519
pmcid: 2707149
Burgess A, Boyd RN, Chatfield MD et al (2021) Hand function in 8- to 12-year-old children with bilateral cerebral palsy and interpretability of the both hands assessment. Phys Occup Ther Pediatr 41(4):358–371. https://doi.org/10.1080/01942638.2020.1856286
doi: 10.1080/01942638.2020.1856286
pubmed: 33334218
Klevberg GL, Østensjø S, Krumlinde-Sundholm L et al (2017) Hand function in a population-based sample of young children with unilateral or bilateral cerebral palsy. Phys Occup Ther Pediatr 37(5):528–540. https://doi.org/10.1080/01942638.2017.1280873
doi: 10.1080/01942638.2017.1280873
pubmed: 28318401
Tinelli F, Guzzetta A, Purpura G et al (2020) Structural brain damage and visual disorders in children with cerebral palsy due to periventricular leukomalacia. Neuroimage Clin 28:102430. https://doi.org/10.1016/j.nicl.2020.102430
doi: 10.1016/j.nicl.2020.102430
pubmed: 32980597
pmcid: 7519396
Coleman A, Fiori S, Weir KA et al (2016) Relationship between brain lesion characteristics and communication in preschool children with cerebral palsy. Res Dev Disabil 58:55–64. https://doi.org/10.1016/j.ridd.2016.08.015
doi: 10.1016/j.ridd.2016.08.015
pubmed: 27591975
Fiori S, Guzzetta A, Pannek K et al (2015) Validity of semi-quantitative scale for brain MRI in unilateral cerebral palsy due to periventricular white matter lesions: relationship with hand sensorimotor function and structural connectivity. Neuroimage Clin 8:104–109. https://doi.org/10.1016/j.nicl.2015.04.005
doi: 10.1016/j.nicl.2015.04.005
pubmed: 26106533
pmcid: 4473818
Iliff JJ, Wang M, Liao Y et al (2012) A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci Transl Med 4(147):147ra111. https://doi.org/10.1126/scitranslmed.3003748
doi: 10.1126/scitranslmed.3003748
pubmed: 22896675
pmcid: 3551275
Harrison IF, Ismail O, Machhada A et al (2020) Impaired glymphatic function and clearance of tau in an Alzheimer’s disease model. Brain 143(8):2576–2593. https://doi.org/10.1093/brain/awaa179
doi: 10.1093/brain/awaa179
pubmed: 32705145
pmcid: 7447521
Xu Z, Xiao N, Chen Y et al (2015) Deletion of aquaporin-4 in APP/PS1 mice exacerbates brain Aβ accumulation and memory deficits. Mol Neurodegener 10:58. https://doi.org/10.1186/s13024-015-0056-1
doi: 10.1186/s13024-015-0056-1
pubmed: 26526066
pmcid: 4631089
Pedersen TJ, Keil SA, Han W et al (2023) The effect of aquaporin-4 mis-localization on Aβ deposition in mice. Neurobiol Dis 181:106100. https://doi.org/10.1016/j.nbd.2023.106100
doi: 10.1016/j.nbd.2023.106100
pubmed: 36990365
Iliff JJ, Chen MJ, Plog BA et al (2014) Impairment of glymphatic pathway function promotes tau pathology after traumatic brain injury. J Neurosci 34(49):16180–16193. https://doi.org/10.1523/jneurosci.3020-14.2014
doi: 10.1523/jneurosci.3020-14.2014
pubmed: 25471560
pmcid: 4252540
Verkhratsky A, Sofroniew MV, Messing A et al (2012) Neurological diseases as primary gliopathies: a reassessment of neurocentrism. ASN Neuro 4(3). https://doi.org/10.1042/an20120010
Iliff JJ, Nedergaard M (2013) Is there a cerebral lymphatic system? Stroke 44(6 Suppl 1):S93–S95. https://doi.org/10.1161/strokeaha.112.678698
doi: 10.1161/strokeaha.112.678698
pubmed: 23709744
pmcid: 3699410
Iliff JJ, Lee H, Yu M et al (2013) Brain-wide pathway for waste clearance captured by contrast-enhanced MRI. J Clin Invest 123(3):1299–1309. https://doi.org/10.1172/jci67677
doi: 10.1172/jci67677
pubmed: 23434588
pmcid: 3582150
Eide PK, Ringstad G (2015) MRI with intrathecal MRI gadolinium contrast medium administration: a possible method to assess glymphatic function in human brain. Acta Radiol Open 4(11):2058460115609635. https://doi.org/10.1177/2058460115609635
doi: 10.1177/2058460115609635
pubmed: 26634147
pmcid: 4652208
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(4):172–178. https://doi.org/10.1007/s11604-017-0617-z
doi: 10.1007/s11604-017-0617-z
pubmed: 28197821
Taoka T, Ito R, Nakamichi R et al (2022) Reproducibility of diffusion tensor image analysis along the perivascular space (DTI-ALPS) for evaluating interstitial fluid diffusivity and glymphatic function: CHanges in Alps index on Multiple conditiON acquIsition eXperiment (CHAMONIX) study. Jpn J Radiol 40(2):147–158. https://doi.org/10.1007/s11604-021-01187-5
doi: 10.1007/s11604-021-01187-5
pubmed: 34390452
Zhang W, Zhou Y, Wang J et al (2021) Glymphatic clearance function in patients with cerebral small vessel disease. Neuroimage 238:118257. https://doi.org/10.1016/j.neuroimage.2021.118257
doi: 10.1016/j.neuroimage.2021.118257
pubmed: 34118396
He P, Shi L, Li Y et al (2023) The association of the glymphatic function with Parkinson’s disease symptoms: neuroimaging evidence from longitudinal and cross-sectional studies. Ann Neurol. https://doi.org/10.1002/ana.26729
Lee HJ, Lee DA, Shin KJ et al (2022) Glymphatic system dysfunction in obstructive sleep apnea evidenced by DTI-ALPS. Sleep Med 89:176–181. https://doi.org/10.1016/j.sleep.2021.12.013
doi: 10.1016/j.sleep.2021.12.013
pubmed: 35030357
Park JH, Bae YJ, Kim JS et al (2023) Glymphatic system evaluation using diffusion tensor imaging in patients with traumatic brain injury. Neuroradiology 65(3):551–557. https://doi.org/10.1007/s00234-022-03073-x
doi: 10.1007/s00234-022-03073-x
pubmed: 36274107
Toh CH, Siow TY (2021) Glymphatic dysfunction in patients with ischemic stroke. Front Aging Neurosci 13:756249. https://doi.org/10.3389/fnagi.2021.756249
doi: 10.3389/fnagi.2021.756249
pubmed: 34819849
pmcid: 8606520
Baxter P, Morris C, Rosenbaum P et al (2007) The definition and classification of cerebral palsy. Dev Med Child Neurol 49(s109):1–44. https://doi.org/10.1111/j.1469-8749.2007.00001.x
Eliasson AC, Krumlinde-Sundholm L, Rösblad B et al (2006) The Manual Ability Classification System (MACS) for children with cerebral palsy: scale development and evidence of validity and reliability. Dev Med Child Neurol 48(7):549–554. https://doi.org/10.1017/s0012162206001162
doi: 10.1017/s0012162206001162
pubmed: 16780622
Holmefur M, Kits A, Bergström J et al (2013) Neuroradiology can predict the development of hand function in children with unilateral cerebral palsy. Neurorehabil Neural Repair 27(1):72–78. https://doi.org/10.1177/1545968312446950
doi: 10.1177/1545968312446950
pubmed: 22677505
Mailleux L, Klingels K, Fiori S et al (2017) How does the interaction of presumed timing, location and extent of the underlying brain lesion relate to upper limb function in children with unilateral cerebral palsy? Eur J Paediatr Neurol 21(5):763–772. https://doi.org/10.1016/j.ejpn.2017.05.006
doi: 10.1016/j.ejpn.2017.05.006
pubmed: 28606752
Basser PJ, Mattiello J, LeBihan D (1994) MR diffusion tensor spectroscopy and imaging. Biophys J 66(1):259–267. https://doi.org/10.1016/s0006-3495(94)80775-1
doi: 10.1016/s0006-3495(94)80775-1
pubmed: 8130344
pmcid: 1275686
Carotenuto A, Cacciaguerra L, Pagani E et al (2022) Glymphatic system impairment in multiple sclerosis: relation with brain damage and disability. Brain 145(8):2785–2795. https://doi.org/10.1093/brain/awab454
doi: 10.1093/brain/awab454
pubmed: 34919648
Rasmussen MK, Mestre H, Nedergaard M (2018) The glymphatic pathway in neurological disorders. Lancet Neurol 17(11):1016–1024. https://doi.org/10.1016/s1474-4422(18)30318-1
doi: 10.1016/s1474-4422(18)30318-1
pubmed: 30353860
pmcid: 6261373
Mallard C, Ek CJ, Vexler ZS (2018) The myth of the immature barrier systems in the developing brain: role in perinatal brain injury. J Physiol 596(23):5655–5664. https://doi.org/10.1113/jp274938
doi: 10.1113/jp274938
pubmed: 29528501
pmcid: 6265562
Stolp HB, Dziegielewska KM (2009) Review: Role of developmental inflammation and blood-brain barrier dysfunction in neurodevelopmental and neurodegenerative diseases. Neuropathol Appl Neurobiol 35(2):132–146. https://doi.org/10.1111/j.1365-2990.2008.01005.x
doi: 10.1111/j.1365-2990.2008.01005.x
pubmed: 19077110
Klostranec JM, Vucevic D, Bhatia KD et al (2021) Current concepts in intracranial interstitial fluid transport and the glymphatic system: part II-imaging techniques and clinical applications. Radiology 301(3):516–532. https://doi.org/10.1148/radiol.2021204088
doi: 10.1148/radiol.2021204088
pubmed: 34698564
Louveau A, Smirnov I, Keyes TJ et al (2015) Structural and functional features of central nervous system lymphatic vessels. Nature 523(7560):337–341. https://doi.org/10.1038/nature14432
doi: 10.1038/nature14432
pubmed: 26030524
pmcid: 4506234
Tzarouchi LC, Astrakas LG, Zikou A et al (2009) Periventricular leukomalacia in preterm children: assessment of grey and white matter and cerebrospinal fluid changes by MRI. Pediatr Radiol 39(12):1327–1332. https://doi.org/10.1007/s00247-009-1389-0
doi: 10.1007/s00247-009-1389-0
pubmed: 19789862
Tzarouchi LC, Xydis V, Zikou AK et al (2011) Diffuse periventricular leukomalacia in preterm children: assessment of grey matter changes by MRI. Pediatr Radiol 41(12):1545–1551. https://doi.org/10.1007/s00247-011-2223-z
doi: 10.1007/s00247-011-2223-z
pubmed: 21901522
Wang M, Iliff JJ, Liao Y et al (2012) Cognitive deficits and delayed neuronal loss in a mouse model of multiple microinfarcts. J Neurosci 32(50):17948–17960. https://doi.org/10.1523/jneurosci.1860-12.2012
doi: 10.1523/jneurosci.1860-12.2012
pubmed: 23238711
pmcid: 3541041
Li W, Chen D, Liu N et al (2022) Modulation of lymphatic transport in the central nervous system. Theranostics 12(3):1117–1131. https://doi.org/10.7150/thno.66026
doi: 10.7150/thno.66026
pubmed: 35154477
pmcid: 8771567
Pagnozzi AM, Dowson N, Doecke J et al (2016) Automated, quantitative measures of grey and white matter lesion burden correlates with motor and cognitive function in children with unilateral cerebral palsy. Neuroimage Clin 11:751–759. https://doi.org/10.1016/j.nicl.2016.05.018
doi: 10.1016/j.nicl.2016.05.018
pubmed: 27330975
pmcid: 4908311
Olsén P, Pääkkö E, Vainionpää L et al (1997) Magnetic resonance imaging of periventricular leukomalacia and its clinical correlation in children. Ann Neurol 41(6):754–761. https://doi.org/10.1002/ana.410410611
doi: 10.1002/ana.410410611
pubmed: 9189036
Sheikh A, Meng X, Liu J et al (2019) Neonatal hypoxia-ischemia causes functional circuit changes in subplate neurons. Cereb Cortex 29(2):765–776. https://doi.org/10.1093/cercor/bhx358
doi: 10.1093/cercor/bhx358
pubmed: 29365081
Liu XB, Shen Y, Pleasure DE et al (2016) The vulnerability of thalamocortical circuitry to hypoxic-ischemic injury in a mouse model of periventricular leukomalacia. BMC Neurosci 17:2. https://doi.org/10.1186/s12868-015-0237-4
doi: 10.1186/s12868-015-0237-4
pubmed: 26733225
pmcid: 4702373
Shen Y, Liu XB, Pleasure DE et al (2012) Axon-glia synapses are highly vulnerable to white matter injury in the developing brain. J Neurosci Res 90(1):105–121. https://doi.org/10.1002/jnr.22722
doi: 10.1002/jnr.22722
pubmed: 21812016
Hoon AH Jr, Stashinko EE, Nagae LM et al (2009) Sensory and motor deficits in children with cerebral palsy born preterm correlate with diffusion tensor imaging abnormalities in thalamocortical pathways. Dev Med Child Neurol 51(9):697–704. https://doi.org/10.1111/j.1469-8749.2009.03306.x
doi: 10.1111/j.1469-8749.2009.03306.x
pubmed: 19416315