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

Qiu-Yue Dong, Tao-Ran Li, Xue-Yan Jiang, Xiao-Ni Wang, Ying Han, Jie-Hui Jiang, Qiu-Yue Dong, Tao-Ran Li, Xue-Yan Jiang, Xiao-Ni Wang, Ying Han, Jie-Hui Jiang

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.

Keywords: Alzheimer’s disease; FDG-PET; Glucose metabolic biomarker; Middle temporal gyrus; Subjective cognitive decline.

Conflict of interest statement

On behalf of all authors, the corresponding author confirms no conflict of interest.

Figures

Fig. 1
Fig. 1
The results of SCD glucose metabolic biomarkers based on ROI analysis. In the metabolic comparisons between SCD patients and NCs, this study considered the 90 regions (AAL template) as ROIs and calculated the mean SUVR value of each ROI, which was adjusted for age, sex, and education. Permutation tests 1000 times were used to find significant differences between NC1 and SCD1 as well as between NC2 and SCD2. a and b show the SCD regional changes of 90 ROIs compared with NC, where a NC1 and SCD1 were used from cohort 1, b NC2 and SCD2 were used from cohort 2, and c shows the intersection areas of significantly different regions in (a) and (b). The regions with metabolic changes of SCD are overlaid on the structural MRI template images. Cool colors represent voxels with negative region weights and hypometabolism, and hot colors represent voxels with positive weights and hypermetabolism. Abbreviations: SCD, subjective cognitive decline; ROI, region of interest; NC, normal control; AAL, anatomical automatic labeling; SUVR, standardized uptake value ratio; MRI, magnetic resonance imaging
Fig. 2
Fig. 2
The metabolism of RMTG in the cognitive continuum. a Plot showing RMTG SUVR of NC2, SCD2, aMCI, ADD, and DLB; b plot showing RMTG SUVR of NC, SCD, aMCI, ADD, and DLB. The SUVR between SCD2 and NC2 (p = 0.034) as well as SCD and NC (p = 0.010) both had significant differences; there were no differences between the ADD and DLB groups (p = 0.227 in a, p = 0.162 in b) but there were significant differences for the remaining combinations (p < 0.001 both in a and b; not marked in Fig. 2). The above p values were all subjected to Bonferroni correction. Abbreviations: RMTG, right middle temporal gyrus; SUVR, standardized uptake value ratio; NC, normal control; SCD, subjective cognitive decline; aMCI, amnestic mild cognitive impairment; ADD, AD-dementia; DLB, dementia with Lewy body
Fig. 3
Fig. 3
The results of correlation analysis. The metabolism of RMTG showed correlations with the scores of SCD-9 (a), HAMD (b), AVLT-N5 (c), and AV45 SUVR (d). More complaints and depression were related to a decreased glucose metabolism of RMTG. AVLT-N5 was positively correlated with RMTG SUVR. The more Aβ deposition, the lower the RMTG metabolism, but it did not reach a significant difference level. Hollow circles indicate NC individuals, solid squares mean SCD individuals, the solid line is the fitted line. Abbreviations: NC, normal control; SCD, subjective cognitive decline; RMTG, right middle temporal gyrus; SUVR, standardized uptake value ratio; SCD-9, Subjective Cognitive Decline-9; HAMD, Hamilton depression scale; AVLT-N5, auditory verbal learning test-long delayed memory; AV45, Florbetapir F-18

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