White matter microstructure and connectivity changes after surgery in male adults with obstructive sleep apnea: recovery or reorganization?

Yaqiong Chai; Hea Ree Park; Hyunjin Jo; Min Young Seo; Hyo Yeol Kim; Eun Yeon Joo; Hosung Kim

doi:10.3389/fnins.2023.1221290

White matter microstructure and connectivity changes after surgery in male adults with obstructive sleep apnea: recovery or reorganization?

Front Neurosci. 2023 Sep 28:17:1221290. doi: 10.3389/fnins.2023.1221290. eCollection 2023.

Authors

Yaqiong Chai^#¹, Hea Ree Park^#², Hyunjin Jo¹, Min Young Seo³, Hyo Yeol Kim⁴, Eun Yeon Joo⁵, Hosung Kim¹

Affiliations

¹ USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine of USC, University of Southern California, Los Angeles, CA, United States.
² Department of Neurology, Inje University College of Medicine, Ilsan Paik Hospital, Goyang, Republic of Korea.
³ Department of Otorhinolaryngology-Head and Neck Surgery, Korea University College of Medicine, Korea University Ansan Hospital, Ansan, Republic of Korea.
⁴ Department of Otorhinolaryngology-Head and Neck Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea.
⁵ Department of Neurology, Neuroscience Center, Samsung Medical Center, Samsung Biomedical Research Institute, School of Medicine, Sungkyunkwan University, Seoul, Republic of Korea.

^# Contributed equally.

Abstract

Study objectives: Obstructive sleep apnea (OSA) is a prevalent clinical problem significantly affecting cognitive functions. Surgical treatment is recommended for those unable to use continuous positive airway pressure. We aimed to investigate the therapeutic effect of upper airway surgery on the white matter (WM) microstructure and brain connectivity in patients with OSA.

Methods: Twenty-one male patients with moderate-to-severe OSA were recruited for multi-level upper airway surgery. Overnight polysomnography (PSG), neuropsychiatric tests, and brain MRI scans were acquired before and 6.1 ± 0.8 months after surgery. Nineteen male patients with untreated OSA were also included as a reference group. We calculated the longitudinal changes of diffusion tensor imaging (DTI) parameters, including fractional anisotropy (ΔFA) and mean/axial/radial diffusivity (ΔMD/AD/RD). We also assessed changes in network properties based on graph theory.

Results: Surgically treated patients showed improvement in PSG parameters and verbal memory after surgery. Globally, ΔFA was significantly higher and ΔRD was lower in the surgery group than in the untreated group. Especially ΔFA of the tracts involved in the limbic system was higher after surgery. In network analysis, higher Δbetweenness and lower Δclustering coefficients were observed in the surgical group than in the untreated group. Finally, the improvement of verbal memory after surgery positively correlated with ΔFA in superior thalamic radiation (p = 0.021), fronto aslant tracts (p = 0.027), and forceps minor tracts (p = 0.032).

Conclusion: Surgical treatment of OSA can alleviate alterations in WM integrity and disruptions in local networks, particularly for the tracts involved in the limbic system. These findings may further explain the cognitive improvement observed after the treatment of OSA.

Keywords: cognitive function; diffusion tensor imaging (DTI); network; obstructive sleep apnea (OSA); upper airway surgery in OSA; white matter (WM).

Grants and funding

P41 EB015922/EB/NIBIB NIH HHS/United States