The Role of Perioperative Sleep Disturbance in Postoperative Neurocognitive Disorders

Xuan Wang, Dongyu Hua, Xiaole Tang, Shan Li, Rao Sun, Zheng Xie, Zhiqiang Zhou, Yilin Zhao, Jintao Wang, Shiyong Li, Ailin Luo, Xuan Wang, Dongyu Hua, Xiaole Tang, Shan Li, Rao Sun, Zheng Xie, Zhiqiang Zhou, Yilin Zhao, Jintao Wang, Shiyong Li, Ailin Luo

Abstract

Postoperative neurocognitive disorder (PND) increases the length of hospital stay, mortality, and risk of long-term cognitive impairment. Perioperative sleep disturbance is prevalent and commonly ignored and may increase the risk of PND. However, the role of perioperative sleep disturbances in PND remains unclear. Nocturnal sleep plays an indispensable role in learning, memory, and maintenance of cerebral microenvironmental homeostasis. Hospitalized sleep disturbances also increase the incidence of postoperative delirium and cognitive dysfunction. This review summarizes the role of perioperative sleep disturbances in PND and elucidates the potential mechanisms underlying sleep-deprivation-mediated PND. Activated neuroinflammation and oxidative stress; impaired function of the blood-brain barrier and glymphatic pathway; decreased hippocampal brain-derived neurotrophic factor, adult neurogenesis, and sirtuin1 expression; and accumulated amyloid-beta proteins are associated with PND in individuals with perioperative sleep disorders. These findings suggest that the improvement of perioperative sleep might reduce the incidence of postoperative delirium and postoperative cognitive dysfunction. Future studies should further investigate the role of perioperative sleep disturbance in PND.

Keywords: cognitive impairment; neuroinflammation; perioperative sleep disturbance; postoperative cognitive dysfunction; postoperative delirium.

Conflict of interest statement

The authors report no conflicts of interest in this work.

© 2021 Wang et al.

Figures

Figure 1
Figure 1
Shared risk factors between preoperative neurocognitive decline and POD and POCD. Shared mechanisms between MCI, AD, POD, and POCD include neuroinflammation, increased amyloid-beta deposition, and disruption of the blood-brain barrier. Common risk factors include advanced age, sleep disorders, and fragility. Moreover, the mutual risk factors for POD and POCD are surgery, anesthesia, and preoperative cognitive decline.
Figure 2
Figure 2
Potential mechanisms of sleep disturbance in postoperative neurocognitive disorders. (A) Signaling pathways associated with sleep deprivation-induced POCD, including neuroinflammation, oxidative stress, elevated biomarkers of aging, disturbed circadian rhythm, and decreased neurotrophic factors. (B) Sleep deprivation leads to several cellular pathological mechanisms in the hippocampus. Complements C3 and C5 in the hippocampus are elevated as a result of sleep deprivation, which activates microglia. Activated microglia further release IL-1β, TNF-α, and IL-6 to exaggerate neuroinflammation. Moreover, sleep deprivation activates neurotoxic astrocytes (A1-specific astrocytes) and weakens astrocytic phagocytosis and their function of synaptic pruning. Activated microglia and astrocytes promote neuronal loss. Sleep deprivation causes decreased spine density of neurons and impaired synaptic plasticity, and decreased BDNF after sleep deprivation also restrains hippocampal adult neurogenesis. All of these cellular pathological changes induced by sleep deprivation accelerate the development of POCD. (C) Structure changes. The blood-brain barrier is damaged by sleep deprivation through decreased tight junctions. Atrophy of the hippocampus and medial prefrontal cortex, as well as decreased hippocampal-prefrontal cortex functional connectivity, may indicate a higher risk of POCD. (D) Dysfunction of the glial-lymphatic pathway. Sleep deprivation causes decreased exchange of the cerebrospinal fluid (CSF) to the interstitial fluid (ISF), which promotes Aβ accumulation. Apolipoprotein E (APOE) in the CSF is reduced after sleep deprivation, resulting in depressed elimination of Aβ. Moreover, advanced age and accumulated Aβ lead to mislocalization of aquaporin 4 (AQP4) expressed in the endfeet of astrocytes, thereby forming a vicious circle to accelerate the development of POCD.

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