Glymphatic system impairment in nonathlete older male adults who played contact sports in their youth associated with cognitive decline: A diffusion tensor image analysis along the perivascular space study

Yuichi Morita; Koji Kamagata; Christina Andica; Kaito Takabayashi; Junko Kikuta; Shohei Fujita; Thomas Samoyeau; Wataru Uchida; Yuya Saito; Hiroki Tabata; Hitoshi Naito; Yuki Someya; Hideyoshi Kaga; Yoshifumi Tamura; Mari Miyata; Toshiaki Akashi; Akihiko Wada; Toshiaki Taoka; Shinji Naganawa; Hirotaka Watada; Ryuzo Kawamori; Osamu Abe; Shigeki Aoki

doi:10.3389/fneur.2023.1100736

Glymphatic system impairment in nonathlete older male adults who played contact sports in their youth associated with cognitive decline: A diffusion tensor image analysis along the perivascular space study

Front Neurol. 2023 Feb 15:14:1100736. doi: 10.3389/fneur.2023.1100736. eCollection 2023.

Authors

Yuichi Morita^{1

2}, Koji Kamagata¹, Christina Andica^{1

3}, Kaito Takabayashi¹, Junko Kikuta¹, Shohei Fujita^{1

2}, Thomas Samoyeau⁴, Wataru Uchida¹, Yuya Saito¹, Hiroki Tabata⁵, Hitoshi Naito⁶, Yuki Someya^{5

7}, Hideyoshi Kaga⁶, Yoshifumi Tamura^{5

6}, Mari Miyata⁸, Toshiaki Akashi¹, Akihiko Wada¹, Toshiaki Taoka⁹, Shinji Naganawa¹⁰, Hirotaka Watada^{5

6}, Ryuzo Kawamori^{5

6}, Osamu Abe², Shigeki Aoki¹

Affiliations

¹ Department of Radiology, Graduate School of Medicine, Juntendo University, Tokyo, Japan.
² Department of Radiology, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan.
³ Faculty of Health Data Science, Juntendo University, Chiba, Japan.
⁴ Department of Radiology, Necker Hospital, Paris University, Paris, France.
⁵ Sportology Center, Graduate School of Medicine, Juntendo University, Tokyo, Japan.
⁶ Department of Metabolism and Endocrinology, Graduate School of Medicine, Juntendo University, Tokyo, Japan.
⁷ Graduate School of Health and Sports Science, Juntendo University, Inzai, Chiba, Japan.
⁸ Department of Functional Brain Imaging, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan.
⁹ Department of Innovative Biomedical Visualization, Graduate School of Medicine, Nagoya University, Nagoya, Japan.
¹⁰ Department of Radiology, Graduate School of Medicine, Nagoya University, Nagoya, Japan.

Abstract

Background and purpose: Exposure to contact sports in youth causes brain health problems later in life. For instance, the repetitive head impacts in contact sports might contribute to glymphatic clearance impairment and cognitive decline. This study aimed to assess the effect of contact sports participation in youth on glymphatic function in old age and the relationship between glymphatic function and cognitive status using the analysis along the perivascular space (ALPS) index.

Materials and methods: A total of 52 Japanese older male subjects were included in the study, including 12 who played heavy-contact sports (mean age, 71.2 years), 15 who played semicontact sports (mean age, 73.1 years), and 25 who played noncontact sports (mean age, 71.3 years) in their youth. All brain diffusion-weighted images (DWIs) of the subjects were acquired using a 3T MRI scanner. The ALPS indices were calculated using a validated semiautomated pipeline. The ALPS indices from the left and right hemispheres were compared between groups using a general linear model, including age and years of education. Furthermore, partial Spearman's rank correlation tests were performed to assess the correlation between the ALPS indices and cognitive scores (Mini-Mental State Examination and the Japanese version of the Montreal Cognitive Assessment [MoCA-J]) after adjusting for age years of education and HbA1c.

Results: The left ALPS index was significantly lower in the heavy-contact and semicontact groups than that in the noncontact group. Although no significant differences were observed in the left ALPS index between the heavy-contact and semicontact groups and in the right ALPS index among groups, a trend toward lower was found in the right ALPS index in individuals with semicontact and heavy-contact compared to the noncontact group. Both sides' ALPS indices were significantly positively correlated with the MoCA-J scores.

Conclusion: The findings indicated the potential adverse effect of contact sports experience in youth on the glymphatic system function in old age associated with cognitive decline.

Keywords: DTI-ALPS; cerebrospinal fluid; contact sports; diffusion-weighted imaging; glymphatic system; interstitial fluid; repetitive head impacts.

Copyright © 2023 Morita, Kamagata, Andica, Takabayashi, Kikuta, Fujita, Samoyeau, Uchida, Saito, Tabata, Naito, Someya, Kaga, Tamura, Miyata, Akashi, Wada, Taoka, Naganawa, Watada, Kawamori, Abe and Aoki.

Grants and funding

This research was supported by the Grants-in-Aid for Scientific Research of the Japan Society for the Promotion of Science (JSPS KAKENHI; Grant Numbers: 19K17244 and 18H02772), the Brain/MINDS Beyond program (Grant Number: JP19dm0307101) of the Japan Agency for Medical Research and Development (AMED), the AMED under Grant Number JP21wm0425006 and JP18dm0307004, 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, and the Juntendo Research Branding Project.