Hypothermia impairs glymphatic drainage in traumatic brain injury as assessed by dynamic contrast-enhanced MRI with intrathecal contrast
IntroductionThe impact of hypothermia on the impaired drainage function of the glymphatic system in traumatic brain injury (TBI) is not understood.MethodsMale Sprague–Dawley rats undergoing controlled cortical impact injury (CCI) were subjected to hypothermia or normothermia treatment. The rats unde...
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Frontiers Media S.A.
2023-02-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2023.1061039/full |
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| author | Wenquan Gu Yingnan Bai Jianguo Cai Honglan Mi Yinghui Bao Xinxin Zhao Chen Lu Fengchen Zhang Yue-hua Li Qing Lu |
| author_facet | Wenquan Gu Yingnan Bai Jianguo Cai Honglan Mi Yinghui Bao Xinxin Zhao Chen Lu Fengchen Zhang Yue-hua Li Qing Lu |
| author_sort | Wenquan Gu |
| collection | DOAJ |
| description | IntroductionThe impact of hypothermia on the impaired drainage function of the glymphatic system in traumatic brain injury (TBI) is not understood.MethodsMale Sprague–Dawley rats undergoing controlled cortical impact injury (CCI) were subjected to hypothermia or normothermia treatment. The rats undergoing sham surgery without CCI were used as the control. Dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) with intrathecal administration of low- and high-molecular-weight contrast agents (Gd-DTPA and hyaluronic acid conjugated Gd-DTPA) was performed after TBI and head temperature management. The semiquantitative kinetic parameters characterizing the contrast infusion and cleanout in the brain, including influx rate, efflux rate, and clearance duration, were calculated from the average time-intensity curves.Results and discussionThe qualitative and semiquantitative results of DCE-MRI obtained from all examined perivascular spaces and most brain tissue regions showed a significantly increased influx rate and efflux rate and decreased clearance duration among all TBI animals, demonstrating a significant impairment of glymphatic drainage function. This glymphatic drainage dysfunction was exacerbated when additional hypothermia was applied. The early glymphatic drainage reduction induced by TBI and aggravated by hypothermia was linearly related to the late increased deposition of p-tau and beta-amyloid revealed by histopathologic and biochemical analysis and cognitive impairment assessed by the Barnes maze and novel object recognition test. The glymphatic system dysfunction induced by hypothermia may be an indirect alternative pathophysiological factor indicating injury to the brain after TBI. Longitudinal studies and targeted glymphatic dysfunction management are recommended to explore the potential effect of hypothermia in TBI. |
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| language | English |
| last_indexed | 2024-04-10T18:14:23Z |
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| spelling | doaj.art-0dc1f082fe304cc3a07955e54bfc4fdd2023-02-02T09:25:13ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2023-02-011710.3389/fnins.2023.10610391061039Hypothermia impairs glymphatic drainage in traumatic brain injury as assessed by dynamic contrast-enhanced MRI with intrathecal contrastWenquan Gu0Yingnan Bai1Jianguo Cai2Honglan Mi3Yinghui Bao4Xinxin Zhao5Chen Lu6Fengchen Zhang7Yue-hua Li8Qing Lu9Department of Radiology, Shanghai Punan Hospital of Pudong New Area, Shanghai, ChinaShanghai Institute of Cardiovascular Diseases, Zhongshan Hospital, Fudan University, Shanghai, ChinaDepartment of Radiology, Xinhua Hospital Chongming Branch, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Radiology, School of Medicine, Renji Hospital, Shanghai Jiao Tong University, Shanghai, ChinaDepartment of Neurology, School of Medicine, Renji Hospital, Shanghai Jiao Tong University, Shanghai, ChinaDepartment of Radiology, School of Medicine, Renji Hospital, Shanghai Jiao Tong University, Shanghai, ChinaShanghai Weiyu International School, Shanghai, ChinaDepartment of Neurology, School of Medicine, Renji Hospital, Shanghai Jiao Tong University, Shanghai, ChinaDepartment of Radiology, Shanghai Sixth People’s Hospital, Shanghai Jiao Tong University, Shanghai, ChinaSchool of Medicine, Shanghai East Hospital, Tongji University, Shanghai, ChinaIntroductionThe impact of hypothermia on the impaired drainage function of the glymphatic system in traumatic brain injury (TBI) is not understood.MethodsMale Sprague–Dawley rats undergoing controlled cortical impact injury (CCI) were subjected to hypothermia or normothermia treatment. The rats undergoing sham surgery without CCI were used as the control. Dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) with intrathecal administration of low- and high-molecular-weight contrast agents (Gd-DTPA and hyaluronic acid conjugated Gd-DTPA) was performed after TBI and head temperature management. The semiquantitative kinetic parameters characterizing the contrast infusion and cleanout in the brain, including influx rate, efflux rate, and clearance duration, were calculated from the average time-intensity curves.Results and discussionThe qualitative and semiquantitative results of DCE-MRI obtained from all examined perivascular spaces and most brain tissue regions showed a significantly increased influx rate and efflux rate and decreased clearance duration among all TBI animals, demonstrating a significant impairment of glymphatic drainage function. This glymphatic drainage dysfunction was exacerbated when additional hypothermia was applied. The early glymphatic drainage reduction induced by TBI and aggravated by hypothermia was linearly related to the late increased deposition of p-tau and beta-amyloid revealed by histopathologic and biochemical analysis and cognitive impairment assessed by the Barnes maze and novel object recognition test. The glymphatic system dysfunction induced by hypothermia may be an indirect alternative pathophysiological factor indicating injury to the brain after TBI. Longitudinal studies and targeted glymphatic dysfunction management are recommended to explore the potential effect of hypothermia in TBI.https://www.frontiersin.org/articles/10.3389/fnins.2023.1061039/fullhypothermia (HT)traumatic brain injuryglymphatic functionmagnetic resonance imaging (MRI)contrast agent |
| spellingShingle | Wenquan Gu Yingnan Bai Jianguo Cai Honglan Mi Yinghui Bao Xinxin Zhao Chen Lu Fengchen Zhang Yue-hua Li Qing Lu Hypothermia impairs glymphatic drainage in traumatic brain injury as assessed by dynamic contrast-enhanced MRI with intrathecal contrast Frontiers in Neuroscience hypothermia (HT) traumatic brain injury glymphatic function magnetic resonance imaging (MRI) contrast agent |
| title | Hypothermia impairs glymphatic drainage in traumatic brain injury as assessed by dynamic contrast-enhanced MRI with intrathecal contrast |
| title_full | Hypothermia impairs glymphatic drainage in traumatic brain injury as assessed by dynamic contrast-enhanced MRI with intrathecal contrast |
| title_fullStr | Hypothermia impairs glymphatic drainage in traumatic brain injury as assessed by dynamic contrast-enhanced MRI with intrathecal contrast |
| title_full_unstemmed | Hypothermia impairs glymphatic drainage in traumatic brain injury as assessed by dynamic contrast-enhanced MRI with intrathecal contrast |
| title_short | Hypothermia impairs glymphatic drainage in traumatic brain injury as assessed by dynamic contrast-enhanced MRI with intrathecal contrast |
| title_sort | hypothermia impairs glymphatic drainage in traumatic brain injury as assessed by dynamic contrast enhanced mri with intrathecal contrast |
| topic | hypothermia (HT) traumatic brain injury glymphatic function magnetic resonance imaging (MRI) contrast agent |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2023.1061039/full |
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