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Erschienen in: European Radiology 11/2018

04.05.2018 | Magnetic Resonance

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

verfasst von: Qiaoyue Tan, Huaiqiang Sun, Weina Wang, Xintong Wu, Nanya Hao, Xiaorui Su, Xibiao Yang, Simin Zhang, Jingkai Su, Qiang Yue, Qiyong Gong

Erschienen in: European Radiology | Ausgabe 11/2018

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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.
Literatur
1.
Zurück zum Zitat 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):4404–4412CrossRef 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):4404–4412CrossRef
2.
Zurück zum Zitat Ranjeva JP, Confort-Gouny S, Le Fur Y et al (2000) Magnetic resonance spectroscopy of brain in epilepsy. Childs Nerv Syst 16(4):235–241CrossRef Ranjeva JP, Confort-Gouny S, Le Fur Y et al (2000) Magnetic resonance spectroscopy of brain in epilepsy. Childs Nerv Syst 16(4):235–241CrossRef
3.
Zurück zum Zitat 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):209–213PubMed 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):209–213PubMed
4.
Zurück zum Zitat 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):1–11CrossRef 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):1–11CrossRef
5.
Zurück zum Zitat 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):825–831CrossRef 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):825–831CrossRef
6.
Zurück zum Zitat 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):2126–2135CrossRef 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):2126–2135CrossRef
7.
Zurück zum Zitat Lieb JP, Dasheiff RM, Engel J Jr (1991) Role of the frontal lobes in the propagation of mesial temporal lobe seizures. Epilepsia 32(6):822–837CrossRef Lieb JP, Dasheiff RM, Engel J Jr (1991) Role of the frontal lobes in the propagation of mesial temporal lobe seizures. Epilepsia 32(6):822–837CrossRef
8.
Zurück zum Zitat 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):453–456 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):453–456
9.
Zurück zum Zitat Hermann B, Seidenberg M, Lee EJ, Chan F, Rutecki P (2007) Cognitive phenotypes in temporal lobe epilepsy. J Int Neuropsychol Soc 13(1):12–20CrossRef Hermann B, Seidenberg M, Lee EJ, Chan F, Rutecki P (2007) Cognitive phenotypes in temporal lobe epilepsy. J Int Neuropsychol Soc 13(1):12–20CrossRef
10.
Zurück zum Zitat Paik E (1998) Functions of the prefrontal cortex in the human brain. J Korean Med Sci 13(6):569–581CrossRef Paik E (1998) Functions of the prefrontal cortex in the human brain. J Korean Med Sci 13(6):569–581CrossRef
11.
Zurück zum Zitat Provencher SW (2001) Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR Biomed 14(4):260–264CrossRef Provencher SW (2001) Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR Biomed 14(4):260–264CrossRef
12.
Zurück zum Zitat Provencher SW (1993) Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med 30(6):672–679CrossRef Provencher SW (1993) Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med 30(6):672–679CrossRef
13.
Zurück zum Zitat 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):545–552CrossRef 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):545–552CrossRef
14.
Zurück zum Zitat 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):e48105CrossRef 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):e48105CrossRef
15.
Zurück zum Zitat 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):369–376CrossRef 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):369–376CrossRef
16.
Zurück zum Zitat 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):1646–1651CrossRef 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):1646–1651CrossRef
17.
Zurück zum Zitat 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):381–389CrossRef 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):381–389CrossRef
18.
Zurück zum Zitat 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):544–553CrossRef 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):544–553CrossRef
19.
Zurück zum Zitat Jayasundar R (2002) Human brain: biochemical lateralization in normal subjects. Neurol India 50(3):267–271PubMed Jayasundar R (2002) Human brain: biochemical lateralization in normal subjects. Neurol India 50(3):267–271PubMed
20.
Zurück zum Zitat 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):2232–2258CrossRef 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):2232–2258CrossRef
21.
Zurück zum Zitat Amunts K, Schlaug G, Schleicher A et al (1996) Asymmetry in the human motor cortex and handedness. Neuroimage 4(3 Pt 1):216–222CrossRef Amunts K, Schlaug G, Schleicher A et al (1996) Asymmetry in the human motor cortex and handedness. Neuroimage 4(3 Pt 1):216–222CrossRef
22.
Zurück zum Zitat 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):1226–1228CrossRef 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):1226–1228CrossRef
23.
Zurück zum Zitat Wellard RM, Briellmann RS, Prichard JW, Syngeniotis A, Jackson GD (2003) Myoinositol abnormalities in temporal lobe epilepsy. Epilepsia 44(6):815–821CrossRef Wellard RM, Briellmann RS, Prichard JW, Syngeniotis A, Jackson GD (2003) Myoinositol abnormalities in temporal lobe epilepsy. Epilepsia 44(6):815–821CrossRef
24.
Zurück zum Zitat Capizzano AA, Vermathen P, Laxer KD et al (2002) Multisection proton MR spectroscopy for mesial temporal lobe epilepsy. AJNR Am J Neuroradiol 23(8):1359–1368PubMedPubMedCentral Capizzano AA, Vermathen P, Laxer KD et al (2002) Multisection proton MR spectroscopy for mesial temporal lobe epilepsy. AJNR Am J Neuroradiol 23(8):1359–1368PubMedPubMedCentral
25.
Zurück zum Zitat 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):355–366CrossRef 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):355–366CrossRef
26.
Zurück zum Zitat 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):603–612CrossRef 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):603–612CrossRef
27.
Zurück zum Zitat 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):195–202CrossRef 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):195–202CrossRef
28.
Zurück zum Zitat Fisher SK, Novak JE, Agranoff BW (2002) Inositol and higher inositol phosphates in neural tissues: homeostasis, metabolism and functional significance. J Neurochem 82(4):736–754CrossRef Fisher SK, Novak JE, Agranoff BW (2002) Inositol and higher inositol phosphates in neural tissues: homeostasis, metabolism and functional significance. J Neurochem 82(4):736–754CrossRef
29.
Zurück zum Zitat 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):576–585CrossRef 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):576–585CrossRef
30.
Zurück zum Zitat Flugel D, McLean MA, Simister RJ, Duncan JS (2006) Magnetisation transfer ratio of choline is reduced following epileptic seizures. NMR Biomed 19(2):217–222CrossRef Flugel D, McLean MA, Simister RJ, Duncan JS (2006) Magnetisation transfer ratio of choline is reduced following epileptic seizures. NMR Biomed 19(2):217–222CrossRef
31.
Zurück zum Zitat 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):976–984CrossRef 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):976–984CrossRef
32.
Zurück zum Zitat 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):1197–1211CrossRef 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):1197–1211CrossRef
33.
Zurück zum Zitat Olsen RW, Avoli M (1997) GABA and epileptogenesis. Epilepsia 38(4):399–407CrossRef Olsen RW, Avoli M (1997) GABA and epileptogenesis. Epilepsia 38(4):399–407CrossRef
34.
Zurück zum Zitat Sherwin A, Robitaille Y, Quesney F et al (1988) Excitatory amino acids are elevated in human epileptic cerebral cortex. Neurology 38(6):920–923CrossRef Sherwin A, Robitaille Y, Quesney F et al (1988) Excitatory amino acids are elevated in human epileptic cerebral cortex. Neurology 38(6):920–923CrossRef
35.
Zurück zum Zitat 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):221–228CrossRef 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):221–228CrossRef
36.
Zurück zum Zitat 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):783–788CrossRef 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):783–788CrossRef
Metadaten
Titel
Quantitative MR spectroscopy reveals metabolic changes in the dorsolateral prefrontal cortex of patients with temporal lobe epilepsy
verfasst von
Qiaoyue Tan
Huaiqiang Sun
Weina Wang
Xintong Wu
Nanya Hao
Xiaorui Su
Xibiao Yang
Simin Zhang
Jingkai Su
Qiang Yue
Qiyong Gong
Publikationsdatum
04.05.2018
Verlag
Springer Berlin Heidelberg
Erschienen in
European Radiology / Ausgabe 11/2018
Print ISSN: 0938-7994
Elektronische ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-018-5443-x

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