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European Radiology

, Volume 28, Issue 11, pp 4496–4503 | Cite as

Quantitative MR spectroscopy reveals metabolic changes in the dorsolateral prefrontal cortex of patients with temporal lobe epilepsy

  • Qiaoyue Tan
  • Huaiqiang Sun
  • Weina Wang
  • Xintong Wu
  • Nanya Hao
  • Xiaorui Su
  • Xibiao Yang
  • Simin Zhang
  • Jingkai Su
  • Qiang Yue
  • Qiyong Gong
Magnetic Resonance
  • 168 Downloads

Abstract

Objective

To characterize possible metabolic changes of the dorsolateral prefrontal cortex (DLPFC) in patients with temporal lobe epilepsy (TLE).

Methods

Quantitative proton magnetic resonance spectroscopy (1H-MRS) studies were performed on 24 TLE patients and 22 healthy controls. Metabolite concentrations were calculated using a linear combination model (LCModel) and corrected for cerebrospinal fluid contamination. Comparisons were performed between the TLE patients and the controls and between the left DLPFC and right DLPFC in each group. Pearson correlation coefficients were calculated between the metabolite concentrations and epilepsy duration and between the metabolite concentrations and voxel tissue composition: [gray matter (GM)/(GM+white matter (WM))].

Results

Metabolic asymmetry was found in controls between the left and right DLPFC, i.e., the NAA concentration of the left DLPFC was significantly higher than that of the right. However, such metabolic asymmetry was not observed in TLE patients. Compared with the controls, TLE patients showed significantly decreased NAA and Ins, and the reductions were greater in the left DLPFC. No significant correlation was found between the metabolite concentrations and epilepsy duration or between the metabolite concentrations and voxel tissue composition [GM/(GM+WM)].

Conclusions

This study suggests that TLE can produce metabolic changes to DLPFC that is remote from the seizure focus.

Key Points

Magnetic resonance spectroscopy probes the brain metabolism noninvasively.

Dorsolateral prefrontal reductions in NAA (a neuronal marker) and Ins are observed in TLE.

Temporal lobe epilepsy can result in metabolic changes remote from the seizure focus.

Keywords

Magnetic resonance spectroscopy Temporal lobe epilepsy Dorsolateral prefrontal cortex Brain Metabolism 

Abbreviations

1H-MRS

Proton magnetic resonance spectroscopy

ANOVA

One-way analysis of variance

ANTs

Advanced normalization tools

CHESS

Chemical shift selective

Cho

Choline, including glycerophosphocholine and phosphocholine

contra

Contralateral to the epileptic focus

Cr

Creatine + phosphocreatine

CSF

Cerebrospinal fluid

DLPFC

Dorsolateral prefrontal cortex

GM

Gray matter

Glx

Glutamate + glutamine

Ins

Myoinositol

ipsi

Ipsilateral to the epileptic focus

L+R

Average value of the left and right DLPFCs

L_sub_TLE

Left TLE subgroup

L

Left

LCModel

Linear combination model

LSD

Least significant difference

MPRAGE

Magnetization prepared rapid gradient echo

NAA

N-acetyl aspartate

PRESS

Point-resolved spectroscopy

R_sub_TLE

Right TLE subgroup

R

Right

TLE

Temporal lobe epilepsy

VOIs

Volumes of interest

WM

White matter

Notes

Acknowledgements

We acknowledge Dr. Richard A.E. Edden for his assistance during the revision of the manuscript.

Funding

This study was funded by National Science Foundation of China (grant nos. 81371528 and 8130118) and the Sichuan Provincial Foundation of Since and Technology (grant no. 2013SZ0047).

Compliance with ethical standards

Guarantor

The scientific guarantor of this publication is Dr. Yue.

Conflict of interest

The authors of this manuscript declare no relationships with any companies.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Ethical approval

Institutional Review Board approval was obtained.

Informed consent

Written informed consent was obtained from all patients in this study.

Methodology

• prospective

• cross-sectional study

• performed at one institution

References

  1. 1.
    Sidek S, Ramli N (2016) In vivo proton magnetic resonance spectroscopy (1H- MRS) evaluation of the metabolite concentration of optic radiation in primary open angle glaucoma. Eur Radiol 26(12):4404–4412CrossRefGoogle Scholar
  2. 2.
    Ranjeva JP, Confort-Gouny S, Le Fur Y et al (2000) Magnetic resonance spectroscopy of brain in epilepsy. Childs Nerv Syst 16(4):235–241CrossRefGoogle Scholar
  3. 3.
    Lu JJ, Ren LK, Feng F et al (2006) Metabolic abnormalities in mesial temporal lobe epilepsy patients depicted by proton MR spectroscopy using a 3. 0t MR scanner. Chin Med Sci J 21(4):209–213PubMedGoogle Scholar
  4. 4.
    Aydin H, Oktay NA, Kizilgoz V, Altin E, Tatar IG, Hekimoglu B (2012) Value of proton-MR-spectroscopy in the diagnosis of temporal lobe epilepsy; correlation of metabolite alterations with electroencephalography. Iran J Radiol 9(1):1–11CrossRefGoogle Scholar
  5. 5.
    Li LM, Dubeau F, Andermann F, Arnold DL (2000) Proton magnetic resonance spectroscopic imaging studies in patients with newly diagnosed partial epilepsy. Epilepsia 41(7):825–831CrossRefGoogle Scholar
  6. 6.
    Krsek P, Hajek M, Dezortova M et al (2007) 1H MR spectroscopic imaging in patients with MRI-negative extratemporal epilepsy: correlation with ictal onset zone and histopathology. Eur Radiol 17(8):2126–2135CrossRefGoogle Scholar
  7. 7.
    Lieb JP, Dasheiff RM, Engel J Jr (1991) Role of the frontal lobes in the propagation of mesial temporal lobe seizures. Epilepsia 32(6):822–837CrossRefGoogle Scholar
  8. 8.
    Drake M, Allegri RF, Thomson A (2000) Executive cognitive alteration of prefrontal type in patients with mesial temporal lobe epilepsy. Medicina (B Aires) 60(4):453–456Google Scholar
  9. 9.
    Hermann B, Seidenberg M, Lee EJ, Chan F, Rutecki P (2007) Cognitive phenotypes in temporal lobe epilepsy. J Int Neuropsychol Soc 13(1):12–20CrossRefGoogle Scholar
  10. 10.
    Paik E (1998) Functions of the prefrontal cortex in the human brain. J Korean Med Sci 13(6):569–581CrossRefGoogle Scholar
  11. 11.
    Provencher SW (2001) Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR Biomed 14(4):260–264CrossRefGoogle Scholar
  12. 12.
    Provencher SW (1993) Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med 30(6):672–679CrossRefGoogle Scholar
  13. 13.
    Hammen T, Hildebrandt M, Stadlbauer A et al (2008) Non-invasive detection of hippocampal sclerosis: correlation between metabolite alterations detected by (1)H-MRS and neuropathology. NMR Biomed 21(6):545–552CrossRefGoogle Scholar
  14. 14.
    Yue Q, Liu M, Nie X et al (2012) Quantitative 3.0T MR spectroscopy reveals decreased creatine concentration in the dorsolateral prefrontal cortex of patients with social anxiety disorder. PLoS One 7(10):e48105CrossRefGoogle Scholar
  15. 15.
    Woermann FG, McLean MA, Bartlett PA, Parker GJ, Barker GJ, Duncan JS (1999) Short echo time single-voxel 1H magnetic resonance spectroscopy in magnetic resonance imaging-negative temporal lobe epilepsy: different biochemical profile compared with hippocampal sclerosis. Ann Neurol 45(3):369–376CrossRefGoogle Scholar
  16. 16.
    Petroff OA, Errante LD, Kim JH, Spencer DD (2003) N-acetyl-aspartate, total creatine, and myo-inositol in the epileptogenic human hippocampus. Neurology 60(10):1646–1651CrossRefGoogle Scholar
  17. 17.
    Bernard D, Walker PM, Baudouin-Poisson N et al (1996) Asymmetric metabolic profile in mesial temporal lobes: localized H-1 MR spectroscopy in healthy right-handed and non-right-handed subjects. Radiology 199(2):381–389CrossRefGoogle Scholar
  18. 18.
    Riederer F, Bittsansky M, Schmidt C et al (2006) 1H magnetic resonance spectroscopy at 3 T in cryptogenic and mesial temporal lobe epilepsy. NMR Biomed 19(5):544–553CrossRefGoogle Scholar
  19. 19.
    Jayasundar R (2002) Human brain: biochemical lateralization in normal subjects. Neurol India 50(3):267–271PubMedGoogle Scholar
  20. 20.
    Rademacher J, Burgel U, Geyer S et al (2001) Variability and asymmetry in the human precentral motor system. A cytoarchitectonic and myeloarchitectonic brain mapping study. Brain 124(Pt 11):2232–2258CrossRefGoogle Scholar
  21. 21.
    Amunts K, Schlaug G, Schleicher A et al (1996) Asymmetry in the human motor cortex and handedness. Neuroimage 4(3 Pt 1):216–222CrossRefGoogle Scholar
  22. 22.
    Gur RC, Packer IK, Hungerbuhler JP et al (1980) Differences in the distribution of gray and white matter in human cerebral hemispheres. Science 207(4436):1226–1228CrossRefGoogle Scholar
  23. 23.
    Wellard RM, Briellmann RS, Prichard JW, Syngeniotis A, Jackson GD (2003) Myoinositol abnormalities in temporal lobe epilepsy. Epilepsia 44(6):815–821CrossRefGoogle Scholar
  24. 24.
    Capizzano AA, Vermathen P, Laxer KD et al (2002) Multisection proton MR spectroscopy for mesial temporal lobe epilepsy. AJNR Am J Neuroradiol 23(8):1359–1368PubMedPubMedCentralGoogle Scholar
  25. 25.
    Mueller SG, Laxer KD, Cashdollar N, Flenniken DL, Matson GB, Weiner MW (2004) Identification of abnormal neuronal metabolism outside the seizure focus in temporal lobe epilepsy. Epilepsia 45(4):355–366CrossRefGoogle Scholar
  26. 26.
    Mueller SG, Ebel A, Barakos J et al (2011) Widespread extrahippocampal NAA/(Cr+Cho) abnormalities in TLE with and without mesial temporal sclerosis. J Neurol 258(4):603–612CrossRefGoogle Scholar
  27. 27.
    Vermathen P, Laxer KD, Schuff N, Matson GB, Weiner MW (2003) Evidence of neuronal injury outside the medial temporal lobe in temporal lobe epilepsy: N-acetylaspartate concentration reductions detected with multisection proton MR spectroscopic imaging--initial experience. Radiology 226(1):195–202CrossRefGoogle Scholar
  28. 28.
    Fisher SK, Novak JE, Agranoff BW (2002) Inositol and higher inositol phosphates in neural tissues: homeostasis, metabolism and functional significance. J Neurochem 82(4):736–754CrossRefGoogle Scholar
  29. 29.
    Brand A, Leibfritz D, Richter-Landsberg C (1999) Oxidative stress-induced metabolic alterations in rat brain astrocytes studied by multinuclear NMR spectroscopy. J Neurosci Res 58(4):576–585CrossRefGoogle Scholar
  30. 30.
    Flugel D, McLean MA, Simister RJ, Duncan JS (2006) Magnetisation transfer ratio of choline is reduced following epileptic seizures. NMR Biomed 19(2):217–222CrossRefGoogle Scholar
  31. 31.
    Lunsing RJ, Strating K, de Koning TJ, Sijens PE (2017) Diagnostic value of MRS-quantified brain tissue lactate level in identifying children with mitochondrial disorders. Eur Radiol 27(3):976–984CrossRefGoogle Scholar
  32. 32.
    Petroff OA, Pleban LA, Spencer DD (1995) Symbiosis between in vivo and in vitro NMR spectroscopy: the creatine, N-acetylaspartate, glutamate, and GABA content of the epileptic human brain. Magn Reson Imaging 13(8):1197–1211CrossRefGoogle Scholar
  33. 33.
    Olsen RW, Avoli M (1997) GABA and epileptogenesis. Epilepsia 38(4):399–407CrossRefGoogle Scholar
  34. 34.
    Sherwin A, Robitaille Y, Quesney F et al (1988) Excitatory amino acids are elevated in human epileptic cerebral cortex. Neurology 38(6):920–923CrossRefGoogle Scholar
  35. 35.
    Westman E, Spenger C, Wahlund LO, Lavebratt C (2007) Carbamazepine treatment recovered low N-acetylaspartate+N-acetylaspartylglutamate (tNAA) levels in the megencephaly mouse BALB/cByJ-Kv1.1(mceph/mceph). Neurobiol Dis 26(1):221–228CrossRefGoogle Scholar
  36. 36.
    Campos BA, Yasuda CL, Castellano G, Bilevicius E, Li LM, Cendes F (2010) Proton MRS may predict AED response in patients with TLE. Epilepsia 51(5):783–788CrossRefGoogle Scholar

Copyright information

© European Society of Radiology 2018

Authors and Affiliations

  • Qiaoyue Tan
    • 1
    • 2
  • Huaiqiang Sun
    • 1
    • 3
  • Weina Wang
    • 1
  • Xintong Wu
    • 4
  • Nanya Hao
    • 4
  • Xiaorui Su
    • 1
  • Xibiao Yang
    • 5
  • Simin Zhang
    • 1
  • Jingkai Su
    • 5
  • Qiang Yue
    • 5
  • Qiyong Gong
    • 1
  1. 1.Huaxi MR Research Center (HMRRC), Department of RadiologyWest China Hospital of Sichuan UniversityChengduPeople’s Republic of China
  2. 2.Division of Radiation Physics, State Key Laboratory of Biotherapy and Cancer CenterWest China Hospital of Sichuan UniversityChengduPeople’s Republic of China
  3. 3.Research Core FacilitiesWest China Hospital of Sichuan UniversityChengduPeople’s Republic of China
  4. 4.Department of NeurologyWest China Hospital of Sichuan UniversityChengduPeople’s Republic of China
  5. 5.Department of RadiologyWest China Hospital of Sichuan UniversityChengduPeople’s Republic of China

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