Share:
Share this content in WeChat
X
Original Article
Mechanism of epidural artery implantation in accelerating the drainage of thalamic interstitial fluid by using tracer-based MRI
ZHOU Jie  LIAN Jingge  REN Qiushi  WANG Hui  KONG Dongsheng  WANG Wei  LIU Huipo  LI Hongfeng  CHENG Jin  HAN Hongbin 

Cite this article as: ZHOU J, LIAN J G, REN Q S, et al. Mechanism of epidural artery implantation in accelerating the drainage of thalamic interstitial fluid by using tracer-based MRI[J]. Chin J Magn Reson Imaging, 2023, 14(2): 97-102. DOI:10.12015/issn.1674-8034.2023.02.017.


[Abstract] Objective To investigate the effect of epidural arterial implantation (EAI) on the drainage of interstitial fluid (ISF) in rat thalamus and its mechanism.Materials and Methods Thirty 240-280 g male SD rats were randomly divided into control group, EAI group and EAI contralateral measurement group. The latter two groups were randomly divided into two subgroups on the 7th and 14th day after operation, with six rats in each group. The ISF drainage in thalamus was detected by tracer-based MRI and using diffusion of extracellular space-mapping (DECS-mapping) techniques to study the structure of extracellular space (ECS). The macroscopic distribution index of ISF drainage: half-life time (T1/2), and the structural parameters of ECS: diffusion rate (D*), tortuosity (λ), volume fraction (α) were obtained. The changes of regional cerebral blood flow in the parietal cortex of rats were observed by laser Doppler flow meter under the guidance of stereotactic instrument. Motor and cognitive performance was quantified with open filed test and novel recognition test at baseline and 7, 14 days after EAI.Results Tracer-based MRI and DECS-mapping analysis showed that the half-life time of EAI7 and EAI14 groups was lower than that of the other groups (P<0.01); the diffusion rate and volume fraction of EAI7 and EAI14 groups increased compared with other groups (P<0.05), and the tortuosity decreased compared with other groups (P<0.05), indicating that the molecular diffusion movement in ECS was accelerated and the structure of ECS was changed. There was no difference in cerebral blood flow between the control group and EAI14 group (P>0.05), indicating that the operation did not change the local cerebral blood flow of rats in a short time. There was no difference in the indexes of animal behavior test among the groups (P>0.05), indicating that the operation did not damage the motor and cognitive abilities of rats.Conclusions EAI changed the microstructure of ECS in the ipsilateral thalamus of rats and promoted the drainage of ISF, which was a stable, safe and effective means of active regulation of brain ECS.
[Keywords] epidural arterial implantation;brain;extracellular space;interstitial fluid;tracer-based magnetic resonance imaging;magnetic resonance imaging

ZHOU Jie1, 2, 3   LIAN Jingge1, 2, 3   REN Qiushi1, 4   WANG Hui1, 2, 3   KONG Dongsheng5   WANG Wei6   LIU Huipo3   LI Hongfeng1   CHENG Jin7*   HAN Hongbin1, 2, 3*  

1 Institute of Medical Technology, Peking University Health Science Center, Beijing 100191, China

2 Department of Radiology, Peking University Third Hospital, Beijing 100191, China

3 Beijing Key Lab of Magnetic Resonance Imaging Device and Technique, Beijing 100191, China

4 Shenzhen Research Institute of Peking University, Shenzhen 518055, China

5 Department of Neurosurgery, First Medical Center, General Hospital of Chinese PLA, Beijing 100191, China

6 Department of Radiology, Beijing Rehabilitation Hospital, Capital Medical University, Beijing 100191, China

7 School of Mathematical Science, Fudan University, Shanghai 200433, China

*Correspondence to: Han HB, E-mail: hanhongbin@bjmu.edu.cn Cheng J, E-mail: jcheng@fudan.edu.cn

Conflicts of interest   None.

ACKNOWLEDGMENTS National Natural Science Foundation of China (No. 12126601); Shenzhen Science and Technology Program (No. KQTD20180412181221912).
Received  2022-10-21
Accepted  2023-01-12
DOI: 10.12015/issn.1674-8034.2023.02.017
Cite this article as: ZHOU J, LIAN J G, REN Q S, et al. Mechanism of epidural artery implantation in accelerating the drainage of thalamic interstitial fluid by using tracer-based MRI[J]. Chin J Magn Reson Imaging, 2023, 14(2): 97-102. DOI:10.12015/issn.1674-8034.2023.02.017.

[1]
GŁADYSZ M Z, STEVANOSKA M, WŁODARCZYK-BIEGUN M K, et al. Breaking through the barrier: modelling and exploiting the physical microenvironment to enhance drug transport and efficacy[J/OL]. Adv Drug Deliv Rev, 2022, 184: 114183 [2022-10-20]. https://www.sciencedirect.com/science/article/pii/S0169409X22000734. DOI: 10.1016/j.addr.2022.114183.
[2]
TAO L C, LIU Q, ZHANG F L, et al. Microglia modulation with 1070-nm light attenuates Aβ burden and cognitive impairment in Alzheimer's disease mouse model[J/OL]. Light Sci Appl, 2021, 10(1): 179 [2022-10-20]. https://www.sciencedirect.com/science/article/pii/S0169409X22000734. DOI: 10.1038/s41377-021-00617-3.
[3]
ABLAT N, LIU R Z, ABLIMIT M, et al. Preventive effects of a standardized flavonoid extract of safflower in rotenone-induced Parkinson's disease rat model[J/OL]. Neuropharmacology, 2022, 217: 109209 [2022-10-20]. https://www.sciencedirect.com/science/article/abs/pii/S0028390822002684. DOI: 10.1016/j.neuropharm.2022.109209.
[4]
GAO Y J, HAN H B, DU J C, et al. Early changes to the extracellular space in the hippocampus under simulated microgravity conditions[J]. Sci China Life Sci, 2022, 65(3): 604-617. DOI: 10.1007/s11427-021-1932-3.
[5]
WANG R, HAN H B, SHI K Y, et al. The alteration of brain interstitial fluid drainage with myelination development[J]. Aging Dis, 2021, 12(7): 1729-1740. DOI: 10.14336/AD.2021.0305.
[6]
MESTRE H, TITHOF J, DU T, et al. Flow of cerebrospinal fluid is driven by arterial pulsations and is reduced in hypertension[J/OL]. Nat Commun, 2018, 9(1): 4878 [2022-10-20]. https://www.nature.com/articles/s41467-018-07318-3. DOI: 10.1038/s41467-018-07318-3.
[7]
TENG Z, WANG A B, WANG P, et al. The effect of aquaporin-4 knockout on interstitial fluid flow and the structure of the extracellular space in the deep brain[J]. Aging Dis, 2018, 9(5): 808-816. DOI: 10.14336/AD.2017.1115.
[8]
XIE L L, KANG H Y, XU Q W, et al. Sleep drives metabolite clearance from the adult brain[J]. Science, 2013, 342(6156): 373-377. DOI: 10.1126/science.1241224.
[9]
SHI Y L, THRIPPLETON M J, BLAIR G W, et al. Small vessel disease is associated with altered cerebrovascular pulsatility but not resting cerebral blood flow[J]. J Cereb Blood Flow Metab, 2020, 40(1): 85-99. DOI: 10.1177/0271678X18803956.
[10]
CAI X J, HE Q Y, WANG W, et al. Epidural pulsation accelerates the drainage of brain interstitial fluid[J]. Aging Dis, 2023, 14(1): 219-228. DOI: 10.14336/ad.2022.0609.
[11]
HAN H B. Discovery of a new division system in brain and the regionalized drainage route of brain interstitial fluid[J]. J Peking Univ Health Sci, 2019, 51(3): 397-401. DOI: 10.19723/j.issn.1671-167X.2019.03.004.
[12]
WANG A B, WANG R, CUI D H, et al. The drainage of interstitial fluid in the deep brain is controlled by the integrity of myelination[J]. Aging Dis, 2019, 10(5): 937-948. DOI: 10.14336/AD.2018.1206.
[13]
HAN H B, LI K, YAN J H, et al. An in vivo study with an MRI tracer method reveals the biophysical properties of interstitial fluid in the rat brain[J]. Sci China Life Sci, 2012, 55(9): 782-787. DOI: 10.1007/s11427-012-4361-4.
[14]
HOU J, WANG W, QUAN X Y, et al. Quantitative visualization of dynamic tracer transportation in the extracellular space of deep brain regions using tracer-based magnetic resonance imaging[J]. Med Sci Monit, 2017, 23: 4260-4268. DOI: 10.12659/msm.903010.
[15]
HAN H B. In vivo quantitative measurement of diffusion parameters in brain extracellular space of rat by using magnetic resonance imaging[J]. J Peking Univ Health Sci, 2012, 44(5): 770-775. DOI: 10.3969/j.issn.1671-167X.2012.05.020.
[16]
WANG W, HE Q Y, HOU J, et al. Stimulation modeling on three-dimensional anisotropic diffusion of MRI tracer in the brain interstitial space[J/OL]. Front Neuroinform, 2019, 13: 6 [2022-10-20]. https://www.frontiersin.org/articles/10.3389/fninf.2019.00006/full. DOI: 10.3389/fninf.2019.00006.
[17]
ILIFF J J, WANG M H, LIAO Y H, et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid Β[J/OL]. Sci Transl Med, 2012, 4(147): 147ra111 [2022-10-20]. https://www.science.org/doi/abs/10.1126/scitranslmed.3003748. DOI: 10.1126/scitranslmed.3003748.
[18]
CHONG P L H, GARIC D, SHEN M D, et al. Sleep, cerebrospinal fluid, and the glymphatic system: a systematic review[J/OL]. Sleep Med Rev, 2022, 61: 101572 [2022-10-20]. https://www.sciencedirect.com/science/article/abs/pii/S108707922100. DOI: 10.1016/j.smrv.2021.101572.
[19]
SHI C Y, LEI Y M, HAN H B, et al. Transportation in the interstitial space of the brain can be regulated by neuronal excitation[J/OL]. Sci Rep, 2015, 5: 17673 [2022-10-20]. https://www.nature.com/articles/srep17673. DOI: 10.1038/srep17673.
[20]
ZHANG Y X, SUN L L, LIU E, et al. The olfactory stimulation slows down the substance clearance in the extracellular space of the hippocampus in rat brain[J]. Biochem Biophys Res Commun, 2019, 515(3): 429-435. DOI: 10.1016/j.bbrc.2019.05.159.
[21]
LI Y Y, HAN H B, SHI K Y, et al. The mechanism of downregulated interstitial fluid drainage following neuronal excitation[J]. Aging Dis, 2020, 11(6): 1407-1422. DOI: 10.14336/AD.2020.0224.
[22]
ZHAO G M, HAN H B, WANG W, et al. Propofol rather than isoflurane accelerates the interstitial fluid drainage in the deep rat brain[J]. Int J Med Sci, 2021, 18(3): 652-659. DOI: 10.7150/ijms.54320.
[23]
ZHAO G M, HAN H B, YANG J, et al. Brain interstitial fluid drainage and extracellular space affected by inhalational isoflurane: in comparison with intravenous sedative dexmedetomidine and pentobarbital sodium[J]. Sci China Life Sci, 2020, 63(9): 1363-1379. DOI: 10.1007/s11427-019-1633-3.
[24]
GRAFF-RADFORD J, YONG K X X, APOSTOLOVA L G, et al. New insights into atypical Alzheimer's disease in the era of biomarkers[J]. Lancet Neurol, 2021, 20(3): 222-234. DOI: 10.1016/S1474-4422(20)30440-3.
[25]
ESPAY A J, LEWITT P A, HAUSER R A, et al. Neurogenic orthostatic hypotension and supine hypertension in Parkinson's disease and related synucleinopathies: prioritisation of treatment targets[J]. Lancet Neurol, 2016, 15(9): 954-966. DOI: 10.1016/S1474-4422(16)30079-5.
[26]
GRINBERG L T, THAL D R. Vascular pathology in the aged human brain[J]. Acta Neuropathol, 2010, 119(3): 277-290. DOI: 10.1007/s00401-010-0652-7.
[27]
NAUEN D W, TRONCOSO J C. Amyloid-beta is present in human lymph nodes and greatly enriched in those of the cervical region[J]. Alzheimers Dement, 2022, 18(2): 205-210. DOI: 10.1002/alz.12385.
[28]
PEROSA V, OLTMER J, MUNTING L P, et al. Perivascular space dilation is associated with vascular amyloid-β accumulation in the overlying cortex[J]. Acta Neuropathol, 2022, 143(3): 331-348. DOI: 10.1007/s00401-021-02393-1.
[29]
CHRISTENSEN J, YAMAKAWA G R, SHULTZ S R, et al. Is the glymphatic system the missing link between sleep impairments and neurological disorders? Examining the implications and uncertainties[J/OL]. Prog Neurobiol, 2021, 198: 101917 [2022-10-20]. https://www.sciencedirect.com/science/article/pii/S0301008220301726. DOI: 10.1016/j.pneurobio.2020.101917.
[30]
NEDERGAARD M, GOLDMAN S A. Glymphatic failure as a final common pathway to dementia[J]. Science, 2020, 370(6512): 50-56. DOI: 10.1126/science.abb8739.
[31]
SALMAN M M, KITCHEN P, HALSEY A, et al. Emerging roles for dynamic aquaporin-4 subcellular relocalization in CNS water homeostasis[J]. Brain, 2022, 145(1): 64-75. DOI: 10.1093/brain/awab311.
[32]
ROCKENSTEIN E, CREWS L, MASLIAH E. Transgenic animal models of neurodegenerative diseases and their application to treatment development[J]. Adv Drug Deliv Rev, 2007, 59(11): 1093-1102. DOI: 10.1016/j.addr.2007.08.013.

PREV Dynamic changes of percent amplitude of fluctuation in sleep deprivation based on resting-state fMRI
NEXT MRI tracer imaging explore the diffusion changes of brain extracellular space in a rat model of intracranial cryptococcal infection
  



Tel & Fax: +8610-67113815    E-mail: editor@cjmri.cn