TY - JOUR
T1 - Spectral quantitative and semi-quantitative EEG provide complementary information on the life-long effects of early childhood malnutrition on cognitive decline
AU - Razzaq, Fuleah A
AU - Calzada-Reyes, Ana
AU - Tang, Qin
AU - Guo, Yanbo
AU - Rabinowitz, Arielle G
AU - Bosch-Bayard, Jorge
AU - Galan-Garcia, Lidice
AU - Virues-Alba, Trinidad
AU - Suarez-Murias, Carlos
AU - Miranda, Ileana
AU - Riaz, Usama
AU - Bernardo Lagomasino, Vivian
AU - Bryce, Cyralene
AU - Anderson, Simon G
AU - Galler, Janina R
AU - Bringas-Vega, Maria L
AU - Valdes-Sosa, Pedro A
N1 - Funding Information:
This research was supported by grants from Nestle Foundation (to MB-V and PV-S, Validation of a long-life neural fingerprint of early malnutrition, 2017), National Institutes of Health (HD060986 to JG), the University of Electronic Sciences and Technology grant Y03111023901014005 and Chengdu Science and Technology Bureau Program under Grant 2022-GH02–00042-HZ to carry out this research.
Publisher Copyright:
Copyright © 2023 Razzaq, Calzada-Reyes, Tang, Guo, Rabinowitz, Bosch-Bayard, Galan-Garcia, Virues-Alba, Suarez-Murias, Miranda, Riaz, Bernardo Lagomasino, Bryce, Anderson, Galler, Bringas-Vega and Valdes-Sosa.
PY - 2023/9/15
Y1 - 2023/9/15
N2 - Objective: This study compares the complementary information from semi-quantitative EEG (sqEEG) and spectral quantitative EEG (spectral-qEEG) to detect the life-long effects of early childhood malnutrition on the brain. Methods: Resting-state EEGs (N = 202) from the Barbados Nutrition Study (BNS) were used to examine the effects of protein-energy malnutrition (PEM) on childhood and middle adulthood outcomes. sqEEG analysis was performed on Grand Total EEG (GTE) protocol, and a single latent variable, the semi-quantitative Neurophysiological State (sqNPS) was extracted. A univariate linear mixed-effects (LME) model tested the dependence of sqNPS and nutritional group. sqEEG was compared with scores on the Montreal Cognitive Assessment (MoCA). Stable sparse classifiers (SSC) also measured the predictive power of sqEEG, spectral-qEEG, and a combination of both. Multivariate LME was applied to assess each EEG modality separately and combined under longitudinal settings. Results: The univariate LME showed highly significant differences between previously malnourished and control groups (p < 0.001); age (p = 0.01) was also significant, with no interaction between group and age detected. Childhood sqNPS (p = 0.02) and adulthood sqNPS (p = 0.003) predicted MoCA scores in adulthood. The SSC demonstrated that spectral-qEEG combined with sqEEG had the highest predictive power (mean AUC 0.92 ± 0.005). Finally, multivariate LME showed that the combined spectral-qEEG+sqEEG models had the highest log-likelihood (−479.7). Conclusion: This research has extended our prior work with spectral-qEEG and the long-term impact of early childhood malnutrition on the brain. Our findings showed that sqNPS was significantly linked to accelerated cognitive aging at 45–51 years of age. While sqNPS and spectral-qEEG produced comparable results, our study indicated that combining sqNPS and spectral-qEEG yielded better performance than either method alone, suggesting that a multimodal approach could be advantageous for future investigations. Significance: Based on our findings, a semi-quantitative approach utilizing GTE could be a valuable diagnostic tool for detecting the lasting impacts of childhood malnutrition. Notably, sqEEG has not been previously explored or reported as a biomarker for assessing the longitudinal effects of malnutrition. Furthermore, our observations suggest that sqEEG offers unique features and information not captured by spectral quantitative EEG analysis and could lead to its improvement.
AB - Objective: This study compares the complementary information from semi-quantitative EEG (sqEEG) and spectral quantitative EEG (spectral-qEEG) to detect the life-long effects of early childhood malnutrition on the brain. Methods: Resting-state EEGs (N = 202) from the Barbados Nutrition Study (BNS) were used to examine the effects of protein-energy malnutrition (PEM) on childhood and middle adulthood outcomes. sqEEG analysis was performed on Grand Total EEG (GTE) protocol, and a single latent variable, the semi-quantitative Neurophysiological State (sqNPS) was extracted. A univariate linear mixed-effects (LME) model tested the dependence of sqNPS and nutritional group. sqEEG was compared with scores on the Montreal Cognitive Assessment (MoCA). Stable sparse classifiers (SSC) also measured the predictive power of sqEEG, spectral-qEEG, and a combination of both. Multivariate LME was applied to assess each EEG modality separately and combined under longitudinal settings. Results: The univariate LME showed highly significant differences between previously malnourished and control groups (p < 0.001); age (p = 0.01) was also significant, with no interaction between group and age detected. Childhood sqNPS (p = 0.02) and adulthood sqNPS (p = 0.003) predicted MoCA scores in adulthood. The SSC demonstrated that spectral-qEEG combined with sqEEG had the highest predictive power (mean AUC 0.92 ± 0.005). Finally, multivariate LME showed that the combined spectral-qEEG+sqEEG models had the highest log-likelihood (−479.7). Conclusion: This research has extended our prior work with spectral-qEEG and the long-term impact of early childhood malnutrition on the brain. Our findings showed that sqNPS was significantly linked to accelerated cognitive aging at 45–51 years of age. While sqNPS and spectral-qEEG produced comparable results, our study indicated that combining sqNPS and spectral-qEEG yielded better performance than either method alone, suggesting that a multimodal approach could be advantageous for future investigations. Significance: Based on our findings, a semi-quantitative approach utilizing GTE could be a valuable diagnostic tool for detecting the lasting impacts of childhood malnutrition. Notably, sqEEG has not been previously explored or reported as a biomarker for assessing the longitudinal effects of malnutrition. Furthermore, our observations suggest that sqEEG offers unique features and information not captured by spectral quantitative EEG analysis and could lead to its improvement.
KW - cognitive decline
KW - EEG
KW - grand total EEG
KW - item response theory
KW - latent variable
KW - malnutrition
KW - qEEG
U2 - 10.3389/fnins.2023.1149102
DO - 10.3389/fnins.2023.1149102
M3 - Article
C2 - 37781256
SN - 1662-4548
VL - 17
JO - Frontiers in Neuroscience
JF - Frontiers in Neuroscience
M1 - 1149102
ER -