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Increased Oxidative Stress Toxicity and Lowered Antioxidant Defenses in Temporal Lobe Epilepsy and Mesial Temporal Sclerosis: Associations with Psychiatric Comorbidities

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Abstract

Oxidative stress toxicity (OSTOX), as well as lowered antioxidant defenses (ANTIOX), plays a role in temporal lobe epilepsy (TLE). Nevertheless, the associations between OSTOX/ANTIOX and psychiatric comorbidities in TLE are largely unknown. Thus, this study examines plasma malondialdehyde (MDA), lipid hydroperoxides (LOOH), advanced oxidation protein products (AOPP), nitric oxide metabolites (NOx), total radical-trapping antioxidant parameter (TRAP), and sulfhydryl (-SH) groups in depression due to TLE (n = 25); anxiety disorders due to TLE (n = 27); psychotic disorder due to TLE (n = 25); “pure TLE” (n = 27); and healthy controls (n = 40). TLE and mesial temporal sclerosis (MTS) were characterized by significant increases in OSTOX (MDA, AOPP, LOOH) and lowered ANTIOX (-SH groups, TRAP). The discrimination of pure TLE from controls yielded a significant area under the ROC curve for MDA (0.999), AOPP (0.851), -SH groups (0.899), and the OSTOX/ANTIOX ratio (0.996). Seizure frequency is significantly associated with increased MDA and lowered LOOH and NOx levels. Increased MDA was associated with the severity of depressive and physiosomatic symptoms, while increased AOPP levels predicted suicidal ideation. Depression and anxiety disorders co-occurring with TLE showed significantly lower MDA levels than TLE without any comorbidities. The psychotic and negative symptoms of TLE are associated with increased MDA levels and excitation with increased LOOH and lowered TRAP levels. These results indicate that oxidative stress toxicity especially protein oxidation and aldehyde formation coupled with lowered -SH groups plays a key role in the pathophysiology of TLE/MTS. Increased aldehyde formation also impacts psychopathology and psychosis, as well as negative and depressive symptoms.

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Abbreviations

TLE:

Temporal lobe epilepsy

MTS:

Mesial temporal sclerosis

GAD:

Generalized anxiety disorder

AEDs:

Antiepileptic drugs

ROS:

Reactive oxygen species

RNS:

Reactive nitrogen species

NO:

Nitric oxide

MDA:

Malondialdehyde

4-HNE:

4-Hydroxynonenal

-SH:

Sulfhydryl

AOPP:

Advanced oxidation protein products

TRAP:

Total radical-trapping antioxidant parameter

LOOH:

Lipid hydroperoxides

MRI:

Magnetic resonance imaging

HAM-D:

Hamilton Depression Rating Scale

HAM-A:

Hamilton Anxiety Rating Scale

BPRS:

Brief Psychiatric Rating Scale

BMI:

Body mass index

NOx :

NO metabolites

OSTOX:

Oxidative stress toxicity index

ANTIOX:

Antioxidant activities index

GLM:

General linear model

FDR:

False discovery rate

ROC:

Receiver operating characteristics

AUC ROC:

Area under the ROC curve

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Funding

The study was supported by the Ratchadapisek Research Funds, Faculty of Medicine, Chulalongkorn University (Grant No. RA 57/024).

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Authors and Affiliations

  1. Department of Psychiatry, Faculty of Medicine, King Chulalongkorn Memorial Hospital, Bangkok, Thailand

    Michael Maes, Thitiporn Supasitthumrong & Buranee Kanchanatawan

  2. Department of Psychiatry, Medical University of Plovdiv, Plovdiv, Bulgaria

    Michael Maes

  3. IMPACT Strategic Research Center, Deakin University, Geelong, Australia

    Michael Maes

  4. Chulalongkorn Comprehensive Epilepsy Center of Excellence (CCEC), The Thai Red Cross Society; Division of Neurology, Department of Medicine, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand

    Chusak Limotai

  5. Health Sciences Graduate Program, Health Sciences Center, State University of Londrina, Londrina, PR, Brazil

    Ana Paula Michelin, Andressa Keiko Matsumoto, Laura de Oliveira Semão, João Victor de Lima Pedrão, Estefânia Gastaldello Moreira & Décio Sabbatini Barbosa

  6. Department of Psychiatry, University of Toronto, Toronto, ON, Canada

    Andre F. Carvalho

  7. Centre for Addiction and Mental Health (CAMH), Toronto, ON, Canada

    Andre F. Carvalho

  8. Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand

    Sunee Sirivichayakul

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  1. Michael Maes
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  2. Thitiporn Supasitthumrong
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Contributions

All the contributing authors have participated in the manuscript. BK and MM designed the study. BK and CL recruited patients and completed diagnostic interviews and rating scale measurements. MM carried out the statistical analyses. All authors contributed to interpretation of the data and writing of the manuscript. All authors approved the final version of the manuscript.

Corresponding author

Correspondence to Buranee Kanchanatawan.

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Maes, M., Supasitthumrong, T., Limotai, C. et al. Increased Oxidative Stress Toxicity and Lowered Antioxidant Defenses in Temporal Lobe Epilepsy and Mesial Temporal Sclerosis: Associations with Psychiatric Comorbidities. Mol Neurobiol 57, 3334–3348 (2020). https://doi.org/10.1007/s12035-020-01949-8

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