Cheng Yanxia, Hu Guangtao, Deng Lin, Zan Yalan, Chen Xia
Department of Pediatrics, Child and Adolescent Psychiatric Center of Jiangbei Campus, The First Affiliated Hospital of Army Medical University (Army 958th Hospital), Chongqing, China.
Front Nutr. 2025 Feb 13;11:1521214. doi: 10.3389/fnut.2024.1521214. eCollection 2024.
Lung injury can lead to specific neurocognitive dysfunction, and the "triple-hit" phenomenon may be the key theoretical mechanism for the progressive impairment of lung injury-related cognitive impairment. The lung and brain can communicate biologically through immune regulation pathway, hypoxic pathway, neural circuit, mitochondrial dysfunction, and microbial influence, which is called the "lung-brain axis." The gut microbiota is a highly complex community of microorganisms that reside in the gut and communicate with the lung via the "gut-lung axis." The dysregulation of gut microbiota may lead to the migration of pathogenic bacteria to the lung, and directly or indirectly regulate the lung immune response through their metabolites, which may cause or aggravate lung injury. The gut microbiota and the brain interact through the "gut-brain axis." The gut microbiota can influence and regulate cognitive function and behavior of the brain through neural pathway mechanisms, immune regulation pathway and hypothalamic-pituitary-adrenal (HPA) axis regulation. Based on the gut microbiota regulation mechanism of the "gut-lung axis" and "gut-brain axis," combined with the mechanisms of cognitive impairment caused by lung injury, we proposed the "triple-hit" hypothesis. It states that the pathophysiological changes of lung injury trigger a series of events such as immune disorder, inflammatory responses, and microbiota changes, which activate the "lung-gut axis," thus forming a "triple-hit" that leads to the development or deterioration of cognitive impairment. This hypothesis provides a more comprehensive framework for studying and understanding brain dysfunction in the context of lung injury. This review proposes the existence of an interactive tandem network for information exchange among the gut, lung, and brain, referred to as the "gut-lung-brain axis." It further explores the potential mechanism of lung injury-related cognitive impairment caused by multiple interactions of gut microbiota in the "gut-lung-brain axis." We found that there are many numerous pathophysiological factors that influence the interaction within the "gut-lung-brain axis." The impact of gut microbiota on cognitive functions related to lung injury may be mediated through mechanisms such as the "triple-hit" hypothesis, direct translocation of microbes and their metabolites, hypoxic pathway, immune modulation, vagal nerve activity, and the HPA axis regulation, among others. As the research deepens, based on the "triple-hit" hypothesis of lung injury, it is further discovered that gut microbial therapy can significantly change the pathogenesis of the inflammatory process on the "gut-lung-brain axis." It can also relieve lung injury and therapeutically modulate brain function and behavior. This perspective provides a new idea for the follow-up treatment of lung injury-related cognitive impairment caused by dysregulation of gut microbiota.
肺损伤可导致特定的神经认知功能障碍,“三重打击”现象可能是肺损伤相关认知障碍进行性损害的关键理论机制。肺和脑可通过免疫调节途径、缺氧途径、神经回路、线粒体功能障碍及微生物影响进行生物学沟通,这被称为“肺-脑轴”。肠道微生物群是存在于肠道内的高度复杂的微生物群落,通过“肠-肺轴”与肺进行沟通。肠道微生物群失调可能导致病原菌迁移至肺,并通过其代谢产物直接或间接调节肺免疫反应,这可能导致或加重肺损伤。肠道微生物群与脑通过“肠-脑轴”相互作用。肠道微生物群可通过神经通路机制、免疫调节途径及下丘脑-垂体-肾上腺(HPA)轴调节影响和调节脑的认知功能及行为。基于“肠-肺轴”和“肠-脑轴”的肠道微生物群调节机制,结合肺损伤所致认知障碍的机制,我们提出了“三重打击”假说。该假说指出,肺损伤的病理生理变化引发一系列事件,如免疫紊乱、炎症反应及微生物群变化,这些事件激活“肺-肠轴”,从而形成导致认知障碍发生或恶化的“三重打击”。这一假说为在肺损伤背景下研究和理解脑功能障碍提供了更全面的框架。本综述提出存在一个肠道、肺和脑之间进行信息交换的交互式串联网络,称为“肠-肺-脑轴”。它进一步探讨了“肠-肺-脑轴”中肠道微生物群多次相互作用导致肺损伤相关认知障碍的潜在机制。我们发现有许多病理生理因素影响“肠-肺-脑轴”内的相互作用。肠道微生物群对与肺损伤相关的认知功能的影响可能通过“三重打击”假说、微生物及其代谢产物的直接移位、缺氧途径、免疫调节、迷走神经活动及HPA轴调节等机制介导。随着研究的深入,基于肺损伤的“三重打击”假说,进一步发现肠道微生物治疗可显著改变“肠-肺-脑轴”上炎症过程的发病机制。它还可减轻肺损伤,并在治疗上调节脑功能及行为。这一观点为肠道微生物群失调所致肺损伤相关认知障碍的后续治疗提供了新思路。