Association of glymphatic system dysfunction with cognitive impairment in temporal lobe epilepsy.

Jiajia Wang, Xiaona Xia, Bin Zhang, Xiaotian Ma, Feng Shi, Ying Wei, Ling Li, Xiangshui Meng
Author Information
  1. Jiajia Wang: Department of Radiology, Qilu Hospital of Shandong University, Jinan, China.
  2. Xiaona Xia: Department of Radiology, Qilu Hospital (Qingdao), Cheeloo College of Medicine, Shandong University, Qingdao, China.
  3. Bin Zhang: Department of Neurology, Qilu Hospital (Qingdao), Cheeloo College of Medicine, Shandong University, Qingdao, China.
  4. Xiaotian Ma: Department of Medicine Experimental Center, Qilu Hospital (Qingdao), Cheeloo College of Medicine, Shandong University, Qingdao, China.
  5. Feng Shi: Department of Research and Development, Shanghai United Imaging Intelligence Co., Ltd., Shanghai, China.
  6. Ying Wei: Department of Research and Development, Shanghai United Imaging Intelligence Co., Ltd., Shanghai, China.
  7. Ling Li: Department of Neurology, Qilu Hospital (Qingdao), Cheeloo College of Medicine, Shandong University, Qingdao, China.
  8. Xiangshui Meng: Department of Radiology, Qilu Hospital (Qingdao), Cheeloo College of Medicine, Shandong University, Qingdao, China.

Abstract

Objectives: To explore the relationship between glymphatic dysfunction and cognitive impairment in unilateral temporal lobe epilepsy (TLE).
Methods: This study retrospectively included 38 patients with unilateral TLE and 26 age- and gender-matched healthy controls (HCs). The diffusion tensor image analysis along the perivascular space (DTI-ALPS) index, choroid plexus volume (CPV), and cognitive assessment were obtained for each participant. Neuropsychological test batteries included Montreal Cognitive Assessment (MoCA), Minimum Mental State Examination, Arithmetic Test (AT), Digit Symbol Substitution Test (DSST), Digit Span Test (DST), Boston Naming Test, Block design, Phonological Fluency Test (PFT), and Semantic Verbal Fluency (SVF).
Results: Compared to HCs, TLE patients had lower scores of MoCA, AT, DSST, DST, Block design, PFT and SVF (all ���<���0.05) and lower values of mean DTI-ALPS index (1.491��������0.142 vs. 1.642��������0.123, ���<���0.001). Significantly lower DTI-ALPS index values were observed in the ipsilateral hemisphere than in the contralateral hemisphere (1.466��������0.129 vs. 1.517��������0.175, ���=���0.013) for patients with unilateral TLE. Correlation analyses found that SVF performance was significantly or borderline significantly associated with glymphatic function (���<���0.05 for all DTI-ALPS index and ���=���0.057 for CPV) in TLE patients. Linear regression analyses showed that increased CPV and decreased DTI-ALPS index were independent risk factors for semantic fluency impairment (all ���<���0.05). Furthermore, mediation analyses found the mediator role of the mean DTI-ALPS index in the relationship between choroid plexus enlargement and semantic fluency impairment (indirect effect: ���=���-0.182, ���=���-0.486 to -0.037).
Conclusion: These findings reveal the important role of the DTI-ALPS index and CPV in SVF performance in unilateral TLE. Decreased DTI-ALPS index and increased CPV are the independent risk factors for semantic fluency impairment. The DTI-ALPS index may fully mediate the relationship between CP enlargement and SVF performance. These insights provide a radiological foundation for further investigations into the mechanism of the glymphatic system in TLE pathophysiology.

Keywords

References

  1. Front Radiol. 2023 Apr 18;3:1153784 [PMID: 37492386]
  2. Mult Scler Relat Disord. 2024 May;85:105550 [PMID: 38493535]
  3. Neuroimage. 2022 Apr 1;249:118830 [PMID: 34965454]
  4. Sci Transl Med. 2012 Aug 15;4(147):147ra111 [PMID: 22896675]
  5. Nat Rev Neurosci. 2007 Dec;8(12):976-87 [PMID: 18026167]
  6. Epilepsia Open. 2024 Feb;9(1):60-76 [PMID: 38041607]
  7. Neuroepidemiology. 2020;54(2):185-191 [PMID: 31852003]
  8. Front Aging Neurosci. 2021 Jul 19;13:693787 [PMID: 34349635]
  9. Alzheimers Res Ther. 2024 Jul 3;16(1):149 [PMID: 38961406]
  10. Lancet Neurol. 2013 Aug;12(8):822-38 [PMID: 23867200]
  11. Oxid Med Cell Longev. 2021 Feb 16;2021:4034509 [PMID: 33680283]
  12. Seizure. 2020 May;78:12-17 [PMID: 32151968]
  13. J Neurosci. 2013 Nov 6;33(45):17553-9 [PMID: 24198345]
  14. J Neurol. 2022 Apr;269(4):2133-2139 [PMID: 34510256]
  15. Neuroimage. 2019 Nov 15;202:116131 [PMID: 31472253]
  16. Stroke. 2020 Sep;51(9):2825-2833 [PMID: 32757750]
  17. Epilepsy Behav. 2015 Aug;49:13-6 [PMID: 25958228]
  18. Eur Radiol. 2023 Sep;33(9):6116-6123 [PMID: 37010581]
  19. Neurology. 2023 May 2;100(18):e1887-e1899 [PMID: 36854619]
  20. Brain Behav. 2020 Jan;10(1):e01475 [PMID: 31863643]
  21. Age Ageing. 2023 Jul 1;52(7): [PMID: 37392401]
  22. Epilepsy Res. 2011 Nov;97(1-2):37-44 [PMID: 21784616]
  23. Neuroradiology. 2023 Dec;65(12):1749-1755 [PMID: 37870589]
  24. Neuropsychologia. 1998 Jun;36(6):499-504 [PMID: 9705059]
  25. J Magn Reson Imaging. 2024 Feb;59(2):431-449 [PMID: 37141288]
  26. Mayo Clin Proc. 1996 Jun;71(6):576-86 [PMID: 8642887]
  27. J Exp Neurosci. 2018 Jul 05;12:1179069518783762 [PMID: 30013386]
  28. Neuroradiology. 2024 Feb;66(2):157-160 [PMID: 38197950]
  29. Neuroimage. 2021 Sep;238:118257 [PMID: 34118396]
  30. Ann Neurol. 2023 Sep;94(3):442-456 [PMID: 37243334]
  31. Neuropsychology. 2000 Jul;14(3):353-60 [PMID: 10928738]
  32. Eur Radiol. 2024 Feb;34(2):1314-1323 [PMID: 37610441]
  33. Acta Radiol Open. 2015 Nov 17;4(11):2058460115609635 [PMID: 26634147]
  34. Ann Neurol. 2023 Jul;94(1):182-195 [PMID: 36971336]
  35. Neurol Neurochir Pol. 2024;58(2):176-184 [PMID: 38324117]
  36. Epilepsia Open. 2022 Jun;7(2):306-314 [PMID: 35305294]
  37. Brain Res. 1979 Jun 29;169(3):590-4 [PMID: 156057]
  38. Curr Opin Neurol. 2018 Aug;31(4):371-378 [PMID: 29782369]
  39. J Neuroradiol. 2023 Nov;50(6):562-567 [PMID: 37301366]
  40. Neurology. 2017 Dec 12;89(24):2462-2468 [PMID: 29117950]
  41. Radiology. 2022 Sep;304(3):635-645 [PMID: 35579521]
  42. Epilepsy Behav. 2008 Feb;12(2):311-6 [PMID: 18082456]
  43. Cortex. 2013 Feb;49(2):528-33 [PMID: 22445445]
  44. Int J Eat Disord. 2023 Feb;56(2):458-463 [PMID: 36367130]
  45. Lancet Neurol. 2007 Nov;6(11):1004-14 [PMID: 17945154]
  46. J Cereb Blood Flow Metab. 2022 Jul;42(7):1163-1175 [PMID: 35296175]
  47. Jpn J Radiol. 2017 Apr;35(4):172-178 [PMID: 28197821]
  48. Sci Rep. 2020 Sep 30;10(1):16144 [PMID: 32999351]
  49. Front Aging Neurosci. 2023 Jul 27;15:1221667 [PMID: 37577357]
  50. Neurology. 2023 Feb 14;100(7):355-356 [PMID: 36781291]
  51. Science. 2013 Oct 18;342(6156):373-7 [PMID: 24136970]
  52. Magn Reson Med Sci. 2024 Jul 1;23(3):268-290 [PMID: 38569866]
  53. J Neurol Neurosurg Psychiatry. 2023 Dec;94(12):1047-1055 [PMID: 37399288]
  54. PLoS One. 2013 Nov 15;8(11):e80713 [PMID: 24348913]
  55. Cereb Cortex. 2009 Nov;19(11):2690-8 [PMID: 19293396]
  56. AJR Am J Roentgenol. 1988 Sep;151(3):559-66 [PMID: 3261518]
  57. Front Neurosci. 2023 Dec 08;17:1312676 [PMID: 38144207]
  58. Parkinsonism Relat Disord. 2021 Aug;89:98-104 [PMID: 34271425]
  59. J Neurol. 2024 Aug;271(8):5598-5609 [PMID: 38913186]
  60. Ann Neurol. 2023 Oct 20;: [PMID: 37860967]
  61. Neuropsychologia. 2005;43(10):1482-92 [PMID: 15989938]
  62. Lancet. 2019 Feb 16;393(10172):689-701 [PMID: 30686584]
  63. Ann Neurol. 2023 Jan;93(1):164-174 [PMID: 36214568]
  64. J Cereb Blood Flow Metab. 1981;1(3):245-66 [PMID: 6276421]
  65. Alzheimers Res Ther. 2016 Dec 5;8(1):52 [PMID: 27915998]
  66. Curr Neurol Neurosci Rep. 2020 Oct 19;20(12):58 [PMID: 33074399]
  67. Seizure. 2009 Jun;18(5):313-9 [PMID: 19186081]
  68. Clin Interv Aging. 2023 May 30;18:855-867 [PMID: 37274869]
  69. Neurosci Lett. 1978 Aug;9(1):77-82 [PMID: 19605197]

Word Cloud

Created with Highcharts 10.0.0DTI-ALPSindexTLEglymphaticimpairmentCPVTestSVFunilateralpatients���<���01semanticfluencysystemrelationshipcognitivetemporallobeepilepsychoroidplexuslower05analysesperformancedysfunctionincludedHCsdiffusiontensorMoCAATDigitDSSTDSTBlockdesignFluencyPFTvaluesmeanvshemisphere���=���0foundsignificantlyincreasedindependentriskfactorsroleenlargement���=���-0Objectives:exploreMethods:studyretrospectively3826age-gender-matchedhealthycontrolsimageanalysisalongperivascularspacevolumeassessmentobtainedparticipantNeuropsychologicaltestbatteriesMontrealCognitiveAssessmentMinimumMentalStateExaminationArithmeticSymbolSubstitutionSpanBostonNamingPhonologicalSemanticVerbalResults:Comparedscores491��������0142642��������0123001Significantlyobservedipsilateralcontralateral466��������0129517��������0175013Correlationborderlineassociatedfunction057LinearregressionshoweddecreasedFurthermoremediationmediatorindirecteffect:182486-0037Conclusion:findingsrevealimportantDecreasedmayfullymediateCPinsightsprovideradiologicalfoundationinvestigationsmechanismpathophysiologyAssociationcentralnervousimaging

Similar Articles

Cited By