Resting-state fMRI network efficiency as a mediator in the relationship between the glymphatic system and cognitive function in obstructive sleep apnea hypopnea syndrome: Insights from a DTI-ALPS investigation

Zhenliang Xiong; Mingxian Bai; Zhongxin Wang; Rongpin Wang; Chong Tian; Lihui Wang; Lisha Nie; Xianchun Zeng

doi:10.1016/j.sleep.2024.05.009

Resting-state fMRI network efficiency as a mediator in the relationship between the glymphatic system and cognitive function in obstructive sleep apnea hypopnea syndrome: Insights from a DTI-ALPS investigation

Sleep Med. 2024 May 3:119:250-257. doi: 10.1016/j.sleep.2024.05.009. Online ahead of print.

Authors

Zhenliang Xiong¹, Mingxian Bai², Zhongxin Wang³, Rongpin Wang², Chong Tian², Lihui Wang⁴, Lisha Nie⁵, Xianchun Zeng⁶

Affiliations

¹ Engineering Research Center of Text Computing & Cognitive Intelligence, Ministry of Education, Key Laboratory of Intelligent Medical Image Analysis and Precise Diagnosis of Guizhou Province, State Key Laboratory of Public Big Data, College of Computer Science and Technology, Guizhou University, Guiyang, China; Department of Radiology, Guizhou Provincial People's Hospital, Key Laboratory of Intelligent Medical Imaging Analysis and Accurate Diagnosis of Guizhou Province, International Exemplary Cooperation Base of Precision Imaging for Diagnosis and Treatment, Guiyang, China.
² Department of Radiology, Guizhou Provincial People's Hospital, Key Laboratory of Intelligent Medical Imaging Analysis and Accurate Diagnosis of Guizhou Province, International Exemplary Cooperation Base of Precision Imaging for Diagnosis and Treatment, Guiyang, China.
³ Department of Pulmonary and Critical Care Medicine, Guizhou Provincial People's Hospital, Guiyang, China.
⁴ Engineering Research Center of Text Computing & Cognitive Intelligence, Ministry of Education, Key Laboratory of Intelligent Medical Image Analysis and Precise Diagnosis of Guizhou Province, State Key Laboratory of Public Big Data, College of Computer Science and Technology, Guizhou University, Guiyang, China.
⁵ GE Healthcare, MR Research China, Beijing, China. Electronic address: nielisa@yeah.net.
⁶ Department of Radiology, Guizhou Provincial People's Hospital, Key Laboratory of Intelligent Medical Imaging Analysis and Accurate Diagnosis of Guizhou Province, International Exemplary Cooperation Base of Precision Imaging for Diagnosis and Treatment, Guiyang, China. Electronic address: zengxianchun04@foxmail.com.

PMID: 38704873
DOI: 10.1016/j.sleep.2024.05.009

Abstract

Introduction: Obstructive sleep apnea hypopnea syndrome (OSAHS) is associated with cognitive impairment and physiological complications, necessitating further understanding of its mechanisms. This study investigates the relationship between glymphatic system function, brain network efficiency, and cognitive impairment in OSAHS patients using diffusion tensor image analysis along the perivascular space (DTI-ALPS) and resting-state fMRI.

Materials and methods: This study included 31 OSAHS patients and 34 age- and gender-matched healthy controls (HC). All participants underwent GE 3.0T magnetic resonance imaging (MRI) with diffusion tensor image (DTI) and resting-state fMRI scans. The DTI-ALPS index and brain functional networks were assessed. Differences between groups and correlations with clinical characteristics were analyzed. Additionally, the mediating role of brain network efficiency was explored. Finally, receiver operating characteristics (ROC) analysis assessed diagnostic performance.

Results: OSAHS patients had significantly lower ALPS-index (1.268 vs. 1.431, p < 0.0001) and moderate negative correlation with Apnea Hypopnea Index (AHI) (r = -0.389, p = 0.031), as well as moderate positive correlation with Montreal Cognitive Assessment (MoCA) (r = 0.525, p = 0.002). Moreover, global efficiency (Eg) of the brain network was positively correlated with the ALPS-index and MoCA scores in OSAHS patients (r = 0.405, p = 0.024; r = 0.56, p = 0.001, respectively). Furthermore, mediation analysis showed that global efficiency partially mediated the impact of glymphatic system dysfunction on cognitive impairment in OSAHS patients (indirect effect = 4.58, mediation effect = 26.9 %). The AUROC for identifying OSAHS and HC was 0.80 (95 % CI 0.69 to 0.91) using an ALPS-index cut-off of 1.35.

Conclusions: OSAHS patients exhibit decreased ALPS-index, indicating impaired glymphatic system function. Dysfunction of the glymphatic system can affect cognitive function in OSAHS by disrupting brain functional network, suggesting a potential underlying pathological mechanism. Additionally, preliminary findings suggest that the ALPS-index may offer promise as a potential indicator for OSAHS.

Keywords: Diffusion tensor image analysis along the perivascular space; Glymphatic system; Graph theory analysis; Mediation analysis; Obstructive sleep apnea hypopnea syndrome.