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Glymphatic system impairment in sleep disruption: diffusion tensor image analysis along the perivascular space (DTI-ALPS)

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Abstract

Purpose

This study aimed to evaluate the relationship between sleep quality as assessed using the Pittsburgh Sleep Quality Index (PSQI) and the index of diffusivity along the perivascular space (ALPS index), a possible indirect indicator of glymphatic system activity.

Materials and methods

This study included the diffusion magnetic resonance imaging (MRI) data of 317 people with sleep disruption and 515 healthy controls (HCs) from the Human Connectome Project (WU-MINN HCP 1200). The ALPS index was calculated automatically based on diffusion tensor image analysis (DTI)-ALPS of diffusion MRI. The ALPS index of the sleep disruption and HC groups was compared using general linear model (GLM) analysis with covariates, such as age, sex, level of education, and intracranial volume. In addition, to confirm the relationship between sleep quality and the ALPS index in the sleep disruption group as well as evaluate the effect of each PSQI component on the ALPS index, correlation analyses between the ALPS indices and PSQI scores of all the components and between the ALPS index and each PSQI component was performed using GLM analysis with the abovementioned covariates, respectively.

Results

The ALPS index was significantly lower in the sleep disruption group than in the HC group (p = 0.001). Moreover, the ALPS indices showed significant negative correlations with the PSQI scores of all the components (false discovery rate [FDR]-corrected p < 0.001). Two significant negative correlations were also found between the ALPS index and PSQI component 2 (sleep latency, FDR-corrected p < 0.001) and 6 (the use of sleep medication, FDR-corrected p < 0.001).

Conclusion

Our findings suggest that glymphatic system impairment contributes to sleep disruption in young adults.

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Acknowledgements

Data were provided (in part) by the Human Connectome Project, WU–Minn Consortium (Principal Investigators: David Van Essen and Kamil Ugurbil; 1U54MH091657) funded by the 16 NIH Institutes and Centers that support the NIH Blueprint for Neuroscience Research, and by the McDonnell Center for Systems Neuroscience at Washington University.

Funding

McDonnell Center for Systems Neuroscience; NIH Blueprint for Neuroscience Research, Grant/Award Number: 1U54MH091657. This study was partially supported by the Juntendo Research Branding Project, JSPS KAKENHI (Grant Nos. 20K16737, 21K07690, 21K12153, 21K15833, 22H04926, 23H02865), a Grant-in-Aid for Special Research in Subsidies for ordinary expenses of private schools from The Promotion and Mutual Aid Corporation for Private Schools of Japan, the Brain/MINDS Beyond program (Grant No. JP19dm0307101) of the Japan Agency for Medical Research and Development (AMED), and AMED under Grant Number JP21wm0425006. The Department of Innovative Biomedical Visualization (iBMV), Nagoya University Graduate School of Medicine, is financially supported by Canon Medical Systems Corporation.

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Author notes

  1. Yuya Saito and Yayoi Hayakawa contributed equally to this work.

Authors and Affiliations

  1. Department of Radiology, Juntendo University Graduate School of Medicine, 2-1-1 Hongo, Bunkyoku, Tokyo, 113-8421, Japan

    Yuya Saito, Yayoi Hayakawa, Koji Kamagata, Junko Kikuta, Christina Andica, Wataru Uchida, Kaito Takabayashi, Rukeye Tuerxun, Zaimire Mahemuti, Takafumi Kitagawa, Takashi Arai, Akiyoshi Suzuki, Kanako Sato, Mitsuo Nishizawa, Toshiaki Akashi, Keigo Shimoji, Akihiko Wada & Shigeki Aoki

  2. Faculty of Health Data Science, Juntendo University, Chiba, Japan

    Takeshi Mita, Christina Andica, Mitsuo Nishizawa & Keigo Shimoji

  3. Department of Innovative Biomedical Visualization (iBMV), Nagoya University Graduate School of Medicine, Nagoya, Japan

    Toshiaki Taoka

  4. Department of Radiological Sciences, Graduate School of Human Health Sciences, Tokyo Metropolitan University, Tokyo, Japan

    Seina Yoshida

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  1. Yuya Saito
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Contributions

YS, YH, and KK conceived the project. YS and YH developed the theory and conducted the experiments. KK and JK provided YS and YH with critical ideas and guidance for the experimental design. All authors contributed to the data interpretation and writing of the final manuscript.

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Correspondence to Koji Kamagata.

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Saito, Y., Hayakawa, Y., Kamagata, K. et al. Glymphatic system impairment in sleep disruption: diffusion tensor image analysis along the perivascular space (DTI-ALPS). Jpn J Radiol 41, 1335–1343 (2023). https://doi.org/10.1007/s11604-023-01463-6

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