Glucose metabolism in the right middle temporal gyrus could be a potential biomarker for subjective cognitive decline: a study of a Han population

Abstract Introduction Subjective cognitive decline (SCD) represents a cognitively normal state but at an increased risk for developing Alzheimer’s disease (AD). Recognizing the glucose metabolic biomarkers of SCD could facilitate the location of areas with metabolic changes at an ultra-early stage....

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Main Authors: Qiu-Yue Dong, Tao-Ran Li, Xue-Yan Jiang, Xiao-Ni Wang, Ying Han, Jie-Hui Jiang
Format: Article
Language:English
Published: BMC 2021-04-01
Series:Alzheimer’s Research & Therapy
Subjects:
Online Access:https://doi.org/10.1186/s13195-021-00811-w
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author Qiu-Yue Dong
Tao-Ran Li
Xue-Yan Jiang
Xiao-Ni Wang
Ying Han
Jie-Hui Jiang
author_facet Qiu-Yue Dong
Tao-Ran Li
Xue-Yan Jiang
Xiao-Ni Wang
Ying Han
Jie-Hui Jiang
author_sort Qiu-Yue Dong
collection DOAJ
description Abstract Introduction Subjective cognitive decline (SCD) represents a cognitively normal state but at an increased risk for developing Alzheimer’s disease (AD). Recognizing the glucose metabolic biomarkers of SCD could facilitate the location of areas with metabolic changes at an ultra-early stage. The objective of this study was to explore glucose metabolic biomarkers of SCD at the region of interest (ROI) level. Methods This study was based on cohorts from two tertiary medical centers, and it was part of the SILCODE project (NCT03370744). Twenty-six normal control (NC) cases and 32 SCD cases were in cohort 1; 36 NCs, 23 cases of SCD, 32 cases of amnestic mild cognitive impairment (aMCIs), 32 cases of AD dementia (ADDs), and 22 cases of dementia with Lewy bodies (DLBs) were in cohort 2. Each subject underwent [18F]fluoro-2-deoxyglucose positron emission tomography (PET) imaging and magnetic resonance imaging (MRI), and subjects from cohort 1 additionally underwent amyloid-PET scanning. The ROI analysis was based on the Anatomical Automatic Labeling (AAL) template; multiple permutation tests and repeated cross-validations were conducted to determine the metabolic differences between NC and SCD cases. In addition, receiver operating characteristic curves were used to evaluate the capabilities of potential glucose metabolic biomarkers in distinguishing different groups. Pearson correlation analysis was also performed to explore the correlation between glucose metabolic biomarkers and neuropsychological scales or amyloid deposition. Results Only the right middle temporal gyrus (RMTG) passed the methodological verification, and its metabolic levels were correlated with the degrees of complaints (R = − 0.239, p = 0.009), depression (R = − 0.200, p = 0.030), and abilities of delayed memory (R = 0.207, p = 0.025), and were weakly correlated with cortical amyloid deposition (R = − 0.246, p = 0.066). Furthermore, RMTG metabolism gradually decreased across the cognitive continuum, and its diagnostic efficiency was comparable (NC vs. ADD, aMCI, or DLB) or even superior (NC vs. SCD) to that of the metabolism of the posterior cingulate cortex or precuneus. Conclusions These findings suggest that the hypometabolism of RMTG could be a typical feature of SCD, and the large-scale hypometabolism in patients with symptomatic stages of AD may start from the RMTG, which gradually progresses starting in the preclinical stage. The specificity of identifying SCD from the perspective of self-perceived symptoms is likely to be increased by the detection of RMTG metabolism.
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spelling doaj.art-e061744c14f74dcdbe0b64003b89ddd32022-12-21T22:39:48ZengBMCAlzheimer’s Research & Therapy1758-91932021-04-0113111210.1186/s13195-021-00811-wGlucose metabolism in the right middle temporal gyrus could be a potential biomarker for subjective cognitive decline: a study of a Han populationQiu-Yue Dong0Tao-Ran Li1Xue-Yan Jiang2Xiao-Ni Wang3Ying Han4Jie-Hui Jiang5Key laboratory of Specialty Fiber Optics and Optical Access Networks, Joint International Research Laboratory of Specialty Fiber Optics and Advanced Communication, School of Information and Communication Engineering, Shanghai UniversityDepartment of Neurology, Xuanwu Hospital of Capital Medical UniversityDepartment of Neurology, Xuanwu Hospital of Capital Medical UniversityDepartment of Neurology, Xuanwu Hospital of Capital Medical UniversityDepartment of Neurology, Xuanwu Hospital of Capital Medical UniversityKey laboratory of Specialty Fiber Optics and Optical Access Networks, Joint International Research Laboratory of Specialty Fiber Optics and Advanced Communication, School of Information and Communication Engineering, Shanghai UniversityAbstract Introduction Subjective cognitive decline (SCD) represents a cognitively normal state but at an increased risk for developing Alzheimer’s disease (AD). Recognizing the glucose metabolic biomarkers of SCD could facilitate the location of areas with metabolic changes at an ultra-early stage. The objective of this study was to explore glucose metabolic biomarkers of SCD at the region of interest (ROI) level. Methods This study was based on cohorts from two tertiary medical centers, and it was part of the SILCODE project (NCT03370744). Twenty-six normal control (NC) cases and 32 SCD cases were in cohort 1; 36 NCs, 23 cases of SCD, 32 cases of amnestic mild cognitive impairment (aMCIs), 32 cases of AD dementia (ADDs), and 22 cases of dementia with Lewy bodies (DLBs) were in cohort 2. Each subject underwent [18F]fluoro-2-deoxyglucose positron emission tomography (PET) imaging and magnetic resonance imaging (MRI), and subjects from cohort 1 additionally underwent amyloid-PET scanning. The ROI analysis was based on the Anatomical Automatic Labeling (AAL) template; multiple permutation tests and repeated cross-validations were conducted to determine the metabolic differences between NC and SCD cases. In addition, receiver operating characteristic curves were used to evaluate the capabilities of potential glucose metabolic biomarkers in distinguishing different groups. Pearson correlation analysis was also performed to explore the correlation between glucose metabolic biomarkers and neuropsychological scales or amyloid deposition. Results Only the right middle temporal gyrus (RMTG) passed the methodological verification, and its metabolic levels were correlated with the degrees of complaints (R = − 0.239, p = 0.009), depression (R = − 0.200, p = 0.030), and abilities of delayed memory (R = 0.207, p = 0.025), and were weakly correlated with cortical amyloid deposition (R = − 0.246, p = 0.066). Furthermore, RMTG metabolism gradually decreased across the cognitive continuum, and its diagnostic efficiency was comparable (NC vs. ADD, aMCI, or DLB) or even superior (NC vs. SCD) to that of the metabolism of the posterior cingulate cortex or precuneus. Conclusions These findings suggest that the hypometabolism of RMTG could be a typical feature of SCD, and the large-scale hypometabolism in patients with symptomatic stages of AD may start from the RMTG, which gradually progresses starting in the preclinical stage. The specificity of identifying SCD from the perspective of self-perceived symptoms is likely to be increased by the detection of RMTG metabolism.https://doi.org/10.1186/s13195-021-00811-wSubjective cognitive declineAlzheimer’s diseaseFDG-PETGlucose metabolic biomarkerMiddle temporal gyrus
spellingShingle Qiu-Yue Dong
Tao-Ran Li
Xue-Yan Jiang
Xiao-Ni Wang
Ying Han
Jie-Hui Jiang
Glucose metabolism in the right middle temporal gyrus could be a potential biomarker for subjective cognitive decline: a study of a Han population
Alzheimer’s Research & Therapy
Subjective cognitive decline
Alzheimer’s disease
FDG-PET
Glucose metabolic biomarker
Middle temporal gyrus
title Glucose metabolism in the right middle temporal gyrus could be a potential biomarker for subjective cognitive decline: a study of a Han population
title_full Glucose metabolism in the right middle temporal gyrus could be a potential biomarker for subjective cognitive decline: a study of a Han population
title_fullStr Glucose metabolism in the right middle temporal gyrus could be a potential biomarker for subjective cognitive decline: a study of a Han population
title_full_unstemmed Glucose metabolism in the right middle temporal gyrus could be a potential biomarker for subjective cognitive decline: a study of a Han population
title_short Glucose metabolism in the right middle temporal gyrus could be a potential biomarker for subjective cognitive decline: a study of a Han population
title_sort glucose metabolism in the right middle temporal gyrus could be a potential biomarker for subjective cognitive decline a study of a han population
topic Subjective cognitive decline
Alzheimer’s disease
FDG-PET
Glucose metabolic biomarker
Middle temporal gyrus
url https://doi.org/10.1186/s13195-021-00811-w
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