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Copyright ©The Author(s) 2025. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Psychiatry. Oct 19, 2025; 15(10): 108861
Published online Oct 19, 2025. doi: 10.5498/wjp.v15.i10.108861
Frontal, temporal, cerebellar changes link to sepsis survivors' cognitive issues: A resting state functional magnetic resonance imaging study
Ying Li, Jian-Qing Chen, Hui Wang, Jian-Jun Yang, Mu-Huo Ji
Ying Li, Jian-Jun Yang, Department of Anesthesiology, Affiliated Zhongda Hospital, School of Medicine, Southeast University, Nanjing 210003, Jiangsu Province, China
Jian-Qing Chen, Department of Anesthesiology, Jiangyin People's Hospital, Affiliated to Nantong University, Jiangyin 214400, Jiangsu Province, China
Hui Wang, Department of Interventional Neurology, The Affiliated Wuxi People's Hospital of Nanjing Medical University, Wuxi 214023, Jiangsu Province, China
Mu-Huo Ji, Department of Anesthesiology, The Second Affiliated Hospital, Nanjing Medical University, Nanjing 210011, Jiangsu Province, China
Co-first authors: Ying Li and Jian-Qing Chen.
Co-corresponding authors: Jian-Jun Yang and Mu-Huo Ji.
Author contributions: Ji MH, Li Y and Chen JQ contributed to research design, data collection, data analysis, and paper writing; Wang H, Li Y and Yang JJ was responsible for research design, funding application, data analysis, reviewing and editing, communication coordination, ethical review, copyright and licensing, and follow-up. Li Y and Chen JQ contributed equally to this work as co-first authors. This manuscript includes two corresponding authors, each of whom played distinct yet complementary roles in the conception, execution, and oversight of this research. Their joint contributions were essential to the study's success. Dr. Yang JJ, serving as the primary doctoral supervisor, provided critical intellectual guidance, oversaw experimental design, and contributed to data interpretation and manuscript development throughout the project. His expertise in neuroinflammation and cognitive impairment was fundamental to the study's scientific rigor and integrity. Dr. Ji MH, as the Principal Investigator (PI), secured the necessary funding, allocated essential resources (including laboratory and core facilities), and established the collaborative framework that enabled this work to proceed. His strategic oversight ensured that the research aligned with the group's long-term vision and objectives in the field of sepsis-related neurological injury and cognitive phenotypes. Both authors jointly supervised the project and share responsibility for communication regarding the integrity and dissemination of the findings. This dual designation accurately reflects their indispensable and complementary contributions to the study's success.
Supported by National Natural Science Foundation of China, No. 82372182, No. 82172131, and No. U23A20421; and Training Project of the Leading Expert Team: "Jiyang Medical Elites", No. RC2023-004.
Institutional review board statement: The research was reviewed and approved by the Medical Ethics Committee of Jiangyin People's Hospital Affiliated with Southeast University.
Informed consent statement: All research participants or their legal guardians provided written informed consent prior to study registration.
Conflict-of-interest statement: No conflict of interest is associated with this work.
Data sharing statement: No other data available.
Open Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Jian-Jun Yang, PhD, Department of Anesthesiology, Affiliated Zhongda Hospital, School of Medicine, Southeast University, No. 87 Dingjiaqiao, Gulou District, Nanjing 210003, Jiangsu Province, China. 15852655431@163.com
Received: April 30, 2025
Revised: June 4, 2025
Accepted: August 8, 2025
Published online: October 19, 2025
Processing time: 148 Days and 24 Hours
Abstract
BACKGROUND

Sepsis is a life-threatening condition defined by organ dysfunction, triggered by a dysregulated host response to infection. there is limited published literature combining cognitive impairment with topological property alterations in brain networks in sepsis survivors. Therefore, we employed graph theory and Granger causality analysis (GCA) methods to analyze resting-state functional magnetic resonance imaging (rs-fMRI) data, aiming to explore the topological alterations in the brain networks of intensive care unit (ICU) sepsis survivors. Using correlation analysis, the interplay between topological property alterations and cognitive impairment was also investigated.

AIM

To explore the topological alterations of the brain networks of sepsis survivors and their correlation with cognitive impairment.

METHODS

Sixteen sepsis survivors and nineteen healthy controls from the community were recruited. Within one month after discharge, neurocognitive tests were administered to assess cognitive performance. Rs-fMRI was acquired and the topological properties of brain networks were measured based on graph theory approaches. GCA was conducted to quantify effective connectivity (EC) between brain regions showing positive topological alterations and other regions in the brain. The correlations between topological properties and cognitive were analyzed.

RESULTS

Sepsis survivors exhibited significant cognitive impairment. At the global level, sepsis survivors showed lower normalized clustering coefficient (γ) and small-worldness (σ) than healthy controls. At the local level, degree centrality (DC) and nodal efficiency (NE) decreased in the right orbital part of inferior frontal gyrus (ORBinf.R), NE decreased in the left temporal pole of superior temporal gyrus (TPOsup.L) whereas DC and NE increased in the right cerebellum Crus 2 (CRBLCrus2.R). Regarding directional connection alterations, EC from left cerebellum 6 (CRBL6.L) to ORBinf.R and EC from TPOsup.L to right cerebellum 1 (CRBLCrus1.R) decreased, whereas EC from right lingual gyrus (LING.R) to TPOsup.L increased. The implementation of correlation analysis revealed a negative correlation between DC in CRBLCrus2.R and both Mini-mental state examination (r = -0.572, P = 0.041) and Montreal cognitive assessment (MoCA) scores (r = -0.629, P = 0.021) at the local level. In the CRBLCrus2.R cohort, a negative correlation was identified between NE and MoCA scores, with a statistically significant result of r = -0.633 and P = 0.020.

CONCLUSION

Frontal, temporal and cerebellar topological property alterations are possibly associated with cognitive impairment of ICU sepsis survivors and may serve as biomarkers for early diagnosis.

Keywords: Sepsis; Cognitive impairment; Functional magnetic resonance imaging; Graph theory; Granger causality analysis; Topological properties

Core Tip: This study innovatively integrates graph theory and Granger causality analysis to uncover distinct topological alterations in frontal, temporal, and cerebellar networks of intensive care unit sepsis survivors. Key findings reveal compensatory hyperconnectivity in the right cerebellum Crus 2, inversely linked to cognitive scores, alongside reduced efficiency in frontal and temporal hubs. Disrupted cerebro-cerebellar directional connectivity further highlights network reorganization post-sepsis. These region-specific network deviations, particularly cerebellar dynamics, offer novel neuroimaging biomarkers for early detection of sepsis-associated cognitive impairment, bridging neuropathological mechanisms with clinical outcomes.