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Published in: Japanese Journal of Radiology 4/2017

01-04-2017 | Original Article

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

Authors: Toshiaki Taoka, Yoshitaka Masutani, Hisashi Kawai, Toshiki Nakane, Kiwamu Matsuoka, Fumihiko Yasuno, Toshifumi Kishimoto, Shinji Naganawa

Published in: Japanese Journal of Radiology | Issue 4/2017

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Abstract

Purpose

The activity of the glymphatic system is impaired in animal models of Alzheimer’s disease (AD). We evaluated the activity of the human glymphatic system in cases of AD with a diffusion-based technique called diffusion tensor image analysis along the perivascular space (DTI-ALPS).

Materials and methods

Diffusion tensor images were acquired to calculate diffusivities in the x, y, and z axes of the plane of the lateral ventricle body in 31 patients. We evaluated the diffusivity along the perivascular spaces as well as projection fibers and association fibers separately, to acquire an index for diffusivity along the perivascular space (ALPS-index) and correlated them with the mini mental state examinations (MMSE) score.

Results

We found a significant negative correlation between diffusivity along the projection fibers and association fibers. We also observed a significant positive correlation between diffusivity along perivascular spaces shown as ALPS-index and the MMSE score, indicating lower water diffusivity along the perivascular space in relation to AD severity.

Conclusion

Activity of the glymphatic system may be evaluated with diffusion images. Lower diffusivity along the perivascular space on DTI-APLS seems to reflect impairment of the glymphatic system. This method may be useful for evaluating the activity of the glymphatic system.
Literature
1.
go back to reference Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci Transl Med. 2012;4(147):147ra11.CrossRef Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci Transl Med. 2012;4(147):147ra11.CrossRef
2.
go back to reference Iliff JJ, Lee H, Yu M, Feng T, Logan J, Nedergaard M, et al. Brain-wide pathway for waste clearance captured by contrast-enhanced MRI. J Clin Invest. 2013;123(3):1299–309.CrossRefPubMedPubMedCentral Iliff JJ, Lee H, Yu M, Feng T, Logan J, Nedergaard M, et al. Brain-wide pathway for waste clearance captured by contrast-enhanced MRI. J Clin Invest. 2013;123(3):1299–309.CrossRefPubMedPubMedCentral
4.
go back to reference Johnston M, Zakharov A, Papaiconomou C, Salmasi G, Armstrong D. Evidence of connections between cerebrospinal fluid and nasal lymphatic vessels in humans, non-human primates and other mammalian species. Cerebrospinal Fluid Res. 2004;1(1):2.CrossRefPubMedPubMedCentral Johnston M, Zakharov A, Papaiconomou C, Salmasi G, Armstrong D. Evidence of connections between cerebrospinal fluid and nasal lymphatic vessels in humans, non-human primates and other mammalian species. Cerebrospinal Fluid Res. 2004;1(1):2.CrossRefPubMedPubMedCentral
5.
go back to reference Murtha LA, Yang Q, Parsons MW, Levi CR, Beard DJ, Spratt NJ, et al. Cerebrospinal fluid is drained primarily via the spinal canal and olfactory route in young and aged spontaneously hypertensive rats. Fluids Barriers CNS. 2014;11:12.CrossRefPubMedPubMedCentral Murtha LA, Yang Q, Parsons MW, Levi CR, Beard DJ, Spratt NJ, et al. Cerebrospinal fluid is drained primarily via the spinal canal and olfactory route in young and aged spontaneously hypertensive rats. Fluids Barriers CNS. 2014;11:12.CrossRefPubMedPubMedCentral
6.
go back to reference Okudera T, Huang YP, Fukusumi A, Nakamura Y, Hatazawa J, Uemura K. Micro-angiographical studies of the medullary venous system of the cerebral hemisphere. Neuropathology. 1999;19(1):93–111.CrossRefPubMed Okudera T, Huang YP, Fukusumi A, Nakamura Y, Hatazawa J, Uemura K. Micro-angiographical studies of the medullary venous system of the cerebral hemisphere. Neuropathology. 1999;19(1):93–111.CrossRefPubMed
7.
go back to reference Reisberg B, Prichep L, Mosconi L, John ER, Glodzik-Sobanska L, Boksay I, et al. The pre-mild cognitive impairment, subjective cognitive impairment stage of Alzheimer’s disease. Alzheimers Dement. 2008;4(1 Suppl 1):S98–108.CrossRefPubMed Reisberg B, Prichep L, Mosconi L, John ER, Glodzik-Sobanska L, Boksay I, et al. The pre-mild cognitive impairment, subjective cognitive impairment stage of Alzheimer’s disease. Alzheimers Dement. 2008;4(1 Suppl 1):S98–108.CrossRefPubMed
8.
go back to reference Masutani Y, Aoki S, Abe O, Hayashi N, Otomo K. MR diffusion tensor imaging: recent advance and new techniques for diffusion tensor visualization. Eur J Radiol. 2003;46(1):53–66.CrossRefPubMed Masutani Y, Aoki S, Abe O, Hayashi N, Otomo K. MR diffusion tensor imaging: recent advance and new techniques for diffusion tensor visualization. Eur J Radiol. 2003;46(1):53–66.CrossRefPubMed
9.
go back to reference Peng W, Achariyar TM, Li B, Liao Y, Mestre H, Hitomi E, et al. Suppression of glymphatic fluid transport in a mouse model of Alzheimer’s disease. Neurobiol Dis. 2016;93:215–25.CrossRefPubMed Peng W, Achariyar TM, Li B, Liao Y, Mestre H, Hitomi E, et al. Suppression of glymphatic fluid transport in a mouse model of Alzheimer’s disease. Neurobiol Dis. 2016;93:215–25.CrossRefPubMed
10.
go back to reference Achariyar TM, Li B, Peng W, Verghese PB, Shi Y, McConnell E, et al. Glymphatic distribution of CSF-derived apoE into brain is isoform specific and suppressed during sleep deprivation. Mol Neurodegener. 2016;11(1):74.CrossRefPubMedPubMedCentral Achariyar TM, Li B, Peng W, Verghese PB, Shi Y, McConnell E, et al. Glymphatic distribution of CSF-derived apoE into brain is isoform specific and suppressed during sleep deprivation. Mol Neurodegener. 2016;11(1):74.CrossRefPubMedPubMedCentral
11.
go back to reference Zeppenfeld DM, Simon M, Haswell JD, D’Abreo D, Murchison C, Quinn JF, et al. Association of perivascular localization of aquaporin-4 with cognition and Alzheimer disease in aging brains. JAMA Neurol. 2016;74(1):91–9.CrossRef Zeppenfeld DM, Simon M, Haswell JD, D’Abreo D, Murchison C, Quinn JF, et al. Association of perivascular localization of aquaporin-4 with cognition and Alzheimer disease in aging brains. JAMA Neurol. 2016;74(1):91–9.CrossRef
12.
go back to reference Tali ET, Ercan N, Krumina G, Rudwan M, Mironov A, Zeng QY, et al. Intrathecal gadolinium (gadopentetate dimeglumine) enhanced magnetic resonance myelography and cisternography: results of a multicenter study. Invest Radiol. 2002;37(3):152–9.CrossRefPubMed Tali ET, Ercan N, Krumina G, Rudwan M, Mironov A, Zeng QY, et al. Intrathecal gadolinium (gadopentetate dimeglumine) enhanced magnetic resonance myelography and cisternography: results of a multicenter study. Invest Radiol. 2002;37(3):152–9.CrossRefPubMed
13.
go back to reference Oner AY, Barutcu B, Aykol S, Tali ET. Intrathecal contrast-enhanced magnetic resonance imaging-related brain signal changes: residual gadolinium deposition? Invest Radiol 2016. doi:10.1097/RLI.0000000000000327 Oner AY, Barutcu B, Aykol S, Tali ET. Intrathecal contrast-enhanced magnetic resonance imaging-related brain signal changes: residual gadolinium deposition? Invest Radiol 2016. doi:10.​1097/​RLI.​0000000000000327​
14.
go back to reference Samardzic D, Thamburaj K. Magnetic resonance characteristics and susceptibility weighted imaging of the brain in gadolinium encephalopathy. J Neuroimaging. 2015;25(1):136–9.CrossRefPubMed Samardzic D, Thamburaj K. Magnetic resonance characteristics and susceptibility weighted imaging of the brain in gadolinium encephalopathy. J Neuroimaging. 2015;25(1):136–9.CrossRefPubMed
15.
go back to reference Naganawa S, Nakane T, Kawai H, Taoka T. Gd-based contrast enhancement of the perivascular spaces in the basal ganglia. Magn Reson Med Sci. 2016;16(1):61–5.CrossRefPubMed Naganawa S, Nakane T, Kawai H, Taoka T. Gd-based contrast enhancement of the perivascular spaces in the basal ganglia. Magn Reson Med Sci. 2016;16(1):61–5.CrossRefPubMed
16.
go back to reference Naganawa S, Suzuki K, Yamazaki M, Sakurai Y. Serial scans in healthy volunteers following intravenous administration of gadoteridol: time course of contrast enhancement in various cranial fluid spaces. Magn Reson Med Sci. 2014;13(1):7–13.CrossRefPubMed Naganawa S, Suzuki K, Yamazaki M, Sakurai Y. Serial scans in healthy volunteers following intravenous administration of gadoteridol: time course of contrast enhancement in various cranial fluid spaces. Magn Reson Med Sci. 2014;13(1):7–13.CrossRefPubMed
17.
go back to reference Taoka T, Fukusumi A, Miyasaka T, Kawai H, Nakane T, Kichikawa K, et al. Structure of the medullary veins of the cerebral hemisphere and related disorders. Radiographics. 2017;37(1):281–97.CrossRefPubMed Taoka T, Fukusumi A, Miyasaka T, Kawai H, Nakane T, Kichikawa K, et al. Structure of the medullary veins of the cerebral hemisphere and related disorders. Radiographics. 2017;37(1):281–97.CrossRefPubMed
18.
go back to reference Fellgiebel A, Yakushev I. Diffusion tensor imaging of the hippocampus in MCI and early Alzheimer’s disease. J Alzheimers Dis. 2011;26(Suppl 3):257–62.PubMed Fellgiebel A, Yakushev I. Diffusion tensor imaging of the hippocampus in MCI and early Alzheimer’s disease. J Alzheimers Dis. 2011;26(Suppl 3):257–62.PubMed
19.
go back to reference Huang H, Fan X, Weiner M, Martin-Cook K, Xiao G, Davis J, et al. Distinctive disruption patterns of white matter tracts in Alzheimer’s disease with full diffusion tensor characterization. Neurobiol Aging. 2012;33(9):2029–45.CrossRefPubMed Huang H, Fan X, Weiner M, Martin-Cook K, Xiao G, Davis J, et al. Distinctive disruption patterns of white matter tracts in Alzheimer’s disease with full diffusion tensor characterization. Neurobiol Aging. 2012;33(9):2029–45.CrossRefPubMed
Metadata
Title
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
Authors
Toshiaki Taoka
Yoshitaka Masutani
Hisashi Kawai
Toshiki Nakane
Kiwamu Matsuoka
Fumihiko Yasuno
Toshifumi Kishimoto
Shinji Naganawa
Publication date
01-04-2017
Publisher
Springer Japan
Published in
Japanese Journal of Radiology / Issue 4/2017
Print ISSN: 1867-1071
Electronic ISSN: 1867-108X
DOI
https://doi.org/10.1007/s11604-017-0617-z

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