MAGNETNO-REZONATNA SPEKTROSKOPIJA MOZGA U MIGRENI
Sažetak
Migrena je čest neurološki poremećaj koji se karakteriše epizodama umerene do teške glavobolje. Magnetno-rezonatna spektroskopija (MRS) je neinvazivna metoda koja omogućuva in vivo proučavanje metabolizma tkiva korišćenjem magnetnih karakteristika određenjih anatomskih jezgara, pre svega vodonika (1H) i fosfora (31P).
1H-MRS se najčešće koristi za merenje koncentracije gama aminobuterne kiseline (GABA), glutamata, fosfokreatina (PCr), kreatina, holina, N-acetilaspartata (NAA), mioinozitola, aspartata i laktata.
31P-MRS omogućava neinvazivno in-vivo merenje koncentracije jedinjenja koja sadrže jezgra fosfora. Ovo omogućava merenje metabolita uključenih u moždani energetski metabolizam uključujući koncentracije fosfokreatina (PCr), neorganskog fosfata, kreatina, adenozin difosfata (ADP) i adenozin trifosfata (ATP).
1H-MRS studije pokazale su signifikantne razlike u nivoima GABA, glutamata, laktata i NAA između pacijenata sa migrenom i kontrolnih grupa, merenih u različitim regionima mozga, dok u većini studija nije pronađena signifikantna razlika u nivoima mioinozitola, holina i ukupnog kreatina.
Glavni konzistentni nalaz u 31P-MRS studijama je konkomitantno smanjenje PCr i povećanje nivoa neorganskog fosfata, odnosno povećanje PCr/neorganski fosfat odnosa, kao i smanjenje nivoa magnezijuma merenih u kortikalnim regionima mozga pacijenata sa migrenom.
Za identifikaciju biomarkera u migreni nephodno je da u budućim studijama budu pribavljene dodatne informacije o iktalnom stanju u migreni kao i o stanju pre i posle terapije. Težina bolesti (trajanje bolesti i frekvencija migrenoznih napada) mora biti uzeta u obzir da bi se detektovala moguća korelacija sa MRS nalazima što takođe zahteva dalje istraživanje.
Reference
Aguila M-ER, Lagopoulos J, Leaver AM, Rebbeck T, Hübscher M, Brennan PC, et al. Elevated levels of GABA+ in migraine detected using (1) H-MRS. NMR Biomed. 2015 Jul;28(7):890-7. [CrossRef] [PubMed]
Akerman S, Holland PR, Goadsby PJ. Diencephalic and brainstem mechanisms in migraine. Nat Rev Neurosci. 2011;12(10):570-84. [CrossRef] [PubMed]
Anttila V, Stefansson H, Kallela M, Todt U, Terwindt GM, Calafato MS, et al. Genome-wide association study of migraine implicates a common susceptibility variant on 8q22.1. Nat Genet. 2010 Oct;42(10):869-73. [CrossRef] [PubMed]
Arngrim N, Schytz HW, Britze J, Amin FM, Vestergaard MB, Hougaard A, et al. Migraine induced by hypoxia: an MRI spectroscopy and angiography study. Brain. 2016 Mar;139(Pt 3):723-37. [CrossRef] [PubMed]
Assarzadegan F, Asgarzadeh S, Hatamabadi HR, Shahrami A, Tabatabaey A, Asgarzadeh M. Serum concentration of magnesium as an independent risk factor in migraine attacks: a matched case-control study and review of the literature. Int Clin Psycho-pharmacol. 2016 Sep;31(5):287-92. [CrossRef] [PubMed]
Aurora SK, Barrodale PM, Tipton RL, Khodavirdi A. Brainstem dysfunction in chronic migraine as evi-denced by neurophysiological and positron emission tomography studies. Headache. 2007;47(7):996-7. [CrossRef] [PubMed]
Barbiroli B, Montagna P, Cortelli P, Funicello R, Iotti S, Monari L, et al. Abnormal brain and muscle energy metabolism shown by 31P magnetic resonance spectroscopy in patients affected by migraine with aura. Neurology. 1992 Jun;42(6):1209-14. [CrossRef] [PubMed]
Barbiroli B, Montagna P, Cortelli P, Martinelli P, Sacquegna T, Zaniol P, et al. Complicated migraine studied by phosphorus magnetic resonance spectro-scopy. Cephalalgia. 1990 Oct;10(5):263-72. [CrossRef] [PubMed]
Baslow MH. N-acetylaspartate in the vertebrate brain: metabolism and function. Neurochem Res. 2003 Jun; 28(6):941-53. [CrossRef] [PubMed]
Bathel A, Schweizer L, Stude P, Glaubitz B, Wulms N, Delice S, et al. Increased thalamic glutamate/ glutamine levels in migraineurs. J Headache Pain. 2018;19(1). [CrossRef] [PubMed]
Becerra L, Veggeberg R, Prescot A, Jensen JE, Renshaw P, Scrivani S, et al. A “complex” of brain metabolites distinguish altered chemistry in the cin-gulate cortex of episodic migraine patients. Neuro-Image Clin. 2016;11:588-94. [CrossRef] [PubMed]
Becerra L, Veggeberg R, Prescot A, Jensen JE, Renshaw P, Scrivani S, et al. A “complex” of brain metabolites distinguish altered chemistry in the cin-gulate cortex of episodic migraine patients. Neuro-Image Clin. 2016;11:588-94. [CrossRef] [PubMed]
Bell T, Stokoe M, Khaira A, Webb M, Noel M, Amoozegar F, et al. GABA and glutamate in pediatric migraine. Pain. 2021;162(1):300-8. [CrossRef] [PubMed]
Bernstein C, Burstein R. Sensitization of the Trige-minovascular Pathway: Perspective and Implications to Migraine Pathophysiology Vascular Theory of Mig-raine- Extracranial Origin Vascular Theory of Migraine- Intracranial Origin. J Clin Neurol. 2012;8:89-99. [CrossRef] [PubMed]
Biermans W, Bakker A, Jacob W. Contact sites be-tween inner and outer mitochondrial membrane: A dynamic microcompartment for creatine kinase acti-vity. Biochim Biophys Acta - Bioenerg. 1990;1018(2): 225-8. [CrossRef] [PubMed]
Bigal ME, Hetherington H, Pan J, Tsang A, Grosberg B, Avdievich N, et al. Occipital levels of GABA are related to severe headaches in migraine. Neurology. 2008 May;70(22):2078-80. [CrossRef] [PubMed]
Boska MD, Welch KM, Barker PB, Nelson JA, Schultz L. Contrasts in cortical magnesium, phospholipid and energy metabolism between migraine syndromes. Headache J Head Face Pain. 2003 Apr 1;43(4):425. [CrossRef] [PubMed]
Boska MD, Welch KMA, Barker PB, Nelson JA, Schultz L. Contrasts in cortical magnesium, phospholipid and energy metabolism between migraine syndromes. Neurology. 2002 Apr;58(8):1227-33. [CrossRef] [PubMed]
Bridge H, Stagg CJ, Near J, Lau C, Zisner A, Cader MZ. Altered neurochemical coupling in the occipital cortex in migraine with visual aura. Cephalalgia. 2015 Oct; 35(11):1025-30. [CrossRef] [PubMed]
Cevoli S, Favoni V, Cortelli P. Energy Metabolism Impairment in Migraine. Curr Med Chem. 2019; 26(34):6253-60. [CrossRef] [PubMed]
Charles AC, Baca SM. Cortical spreading depression and migraine. Nat Rev Neurol. 2013 Nov;9(11):637-44. [CrossRef] [PubMed]
Chasman DI, Schürks M, Anttila V, de Vries B, Schminke U, Launer LJ, et al. Genome-wide asso-ciation study reveals three susceptibility loci for com-mon migraine in the general population. Nat Genet. 2011 Jun;43(7):695-8. [CrossRef] [PubMed]
Choi C, Coupland NJ, Bhardwaj PP, Kalra S, Casault CA, Reid K, et al. T2 measurement and quantification of glutamate in human brain in vivo. Magn Reson Med. 2006;56(5):971-7. [CrossRef] [PubMed]
Christiansen P, Henriksen O, Stubgaard M, Gideon P, Larsson HB. In vivo quantification of brain metabolites by 1H-MRS using water as an internal standard. Magn Reson Imaging. 1993;11(1):107-18. [CrossRef] [PubMed]
Clark JB. N-acetyl aspartate: a marker for neuronal loss or mitochondrial dysfunction. Dev Neurosci. 1998; 20(4-5):271-6. [CrossRef] [PubMed]
Cozzolino O, Marchese M, Trovato F, Pracucci E, Ratto GM, Buzzi MG, et al. Understanding spreading de-pression from headache to sudden unexpected death. Front Neurol. 2018;9(FEB):1-13. [CrossRef] [PubMed]
de Tommaso M, Ceci E, Pica C, Trojano M, Delussi M, Franco G, et al. Serum levels of N-acetyl-aspartate in migraine and tension-type headache. J Headache Pain. 2012 Jul;13(5):389-94. [CrossRef] [PubMed]
Dichgans M, Herzog J, Freilinger T, Wilke M, Auer DP. 1H-MRS alterations in the cerebellum of patients with familial hemiplegic migraine type 1. Neurology. 2005 Feb;64(4):608-13. [CrossRef] [PubMed]
Diener H-C, Charles A, Goadsby PJ, Holle D. New therapeutic approaches for the prevention and treat-ment of migraine. Lancet Neurol. 2015 Oct;14(10): 1010-22. [CrossRef] [PubMed]
Enna SJ, McCarson KE. The role of GABA in the mediation and perception of pain. Adv Pharmacol. 2006;54:1-27. [CrossRef] [PubMed]
Fayed N, Andrés E, Viguera L, Modrego PJ, Garcia-Campayo J. Higher glutamate+glutamine and reduc-tion of N-acetylaspartate in posterior cingulate ac-cording to age range in patients with cognitive impair-ment and/or pain. Acad Radiol. 2014 Sep;21(9): 1211-7. [CrossRef] [PubMed]
Ferroni P, Barbanti P, Spila A, Fratangeli F, Aurilia C, Fofi L, et al. Circulating Biomarkers in Migraine: New Opportunities for Precision Medicine. Curr Med Chem. 2018;26(34):6191-206. [CrossRef] [PubMed]
Gantenbein AR, Sandor PS, Fritschy J, Turner R, Goadsby PJ, Kaube H. Sensory information processing may be neuroenergetically more demanding in mig-raine patients. Neuroreport. 2013;24(4). [CrossRef] [PubMed]
García-Martín E, Ramos MI, Cornejo-García JA, Galván S, Perkins JR, Rodríguez-Santos L, et al. Missense Gamma-Aminobutyric Acid Receptor Polymorphisms Are Associated with Reaction Time, Motor Time, and Ethanol Effects in Vivo. Vol. 12, Frontiers in Cellular Neuroscience. 2018. p. 10. [CrossRef] [PubMed]
González de la Aleja J, Ramos A, Mato-Abad V, Martínez-Salio A, Hernández-Tamames JA, Molina JA, et al. Higher glutamate to glutamine ratios in occipital regions in women with migraine during the interictal state. Headache. 2013 Feb;53(2):365-75. [CrossRef] [PubMed]
González De La Aleja J, Ramos A, Mato-Abad V, Martínez-Salio A, Hernández-Tamames JA, Molina JA, et al. Higher glutamate to glutamine ratios in occipital regions in women with migraine during the interictal state. Headache. 2013;53(2):365-75. [CrossRef] [PubMed]
Grimaldi D, Tonon C, Cevoli S, Pierangeli G, Malucelli E, Rizzo G, et al. Clinical and neuroimaging evidence of interictal cerebellar dysfunction in FHM2. Cepha-lalgia. 2010 May;30(5):552-9. [CrossRef] [PubMed]
Gross EC, Lisicki M, Fischer D, Sándor PS, Schoenen J. The metabolic face of migraine — from pathophysio-logy to treatment. Nat Rev Neurol. 2019;15(11): 627-43. [CrossRef] [PubMed]
Gu T, Ma X-X, Xu Y-H, Xiu J-J, Li C-F. Metabolite con-centration ratios in thalami of patients with migraine and trigeminal neuralgia measured with 1H-MRS. Neurol Res. 2008 Apr;30(3):229-33. [CrossRef] [PubMed]
Jansen JFA, Backes WH, Nicolay K, Kooi ME. 1H MR spectroscopy of the brain: absolute quantification of metabolites. Radiology. 2006 Aug;240(2):318-32. [CrossRef] [PubMed]
Jourdain P, Allaman I, Rothenfusser K, Fiumelli H, Marquet P, Magistretti PJ. L-Lactate protects neurons against excitotoxicity: implication of an ATP-mediated signaling cascade. Sci Rep. 2016;6(1):21250. [CrossRef] [PubMed]
Kim JH, Kim S, Suh S-I, Koh S-B, Park K-W, Oh K. Interictal metabolic changes in episodic migraine: a voxel-based FDG-PET study. Cephalalgia. 2010 Jan; 30(1):53-61. [CrossRef] [PubMed]
Kocharyan A, Fernandes P, Tong X-K, Vaucher E, Hamel E. Specific subtypes of cortical GABA inter-neurons contribute to the neurovascular coupling res-ponse to basal forebrain stimulation. J Cereb blood flow Metab Off J Int Soc Cereb Blood Flow Metab. 2008 Feb;28(2):221-31. [CrossRef] [PubMed]
Kupers R, Danielsen ER, Kehlet H, Christensen R, Thomsen C. Painful tonic heat stimulation induces GABA accumulation in the prefrontal cortex in man. Pain. 2009 Mar;142(1-2):89-93. [CrossRef] [PubMed]
Lai T-H, Chou K-H, Fuh J-L, Lee P-L, Kung Y-C, Lin C-P, et al. Gray matter changes related to medication overuse in patients with chronic migraine. Cephalalgia. 2016 Dec;36(14):1324-33. [CrossRef] [PubMed]
Lai T-H, Fuh J-L, Lirng J-F, Lin C-P, Wang S-J. Brain-stem 1H-MR spectroscopy in episodic and chronic migraine. J Headache Pain. 2012 Nov;13(8):645-51. [CrossRef] [PubMed]
Lauritzen M, Hansen AJ. The effect of glutamate receptor blockade on anoxic depolarization and cortical spreading depression. J Cereb blood flow Metab Off J Int Soc Cereb Blood Flow Metab. 1992 Mar;12(2): 223-9. [CrossRef] [PubMed]
Li Q, Chen C, Gong T. High-field MRS study of GABA+ in patients with migraine: Response to levetiracetam treatment. Neuroreport. 2018;29(12):1007-10. [CrossRef] [PubMed]
Lirng J-F, Chen H-C, Fuh J-L, Tsai C-F, Liang J-F, Wang S-J. Increased myo-inositol level in dorsolateral prefrontal cortex in migraine patients with major de-pression. Cephalalgia. 2015 Jul;35(8):702-9. [CrossRef] [PubMed]
Lodi R, Iotti S, Cortelli P, Pierangeli G, Cevoli S, Clementi V, et al. Deficient energy metabolism is associated with low free magnesium in the brains of patients with migraine and cluster headache. Brain Res Bull. 2001 Mar;54(4):437-41. [CrossRef] [PubMed]
Lodi R, Kemp GJ, Montagna P, Pierangeli G, Cortelli P, Iotti S, et al. Quantitative analysis of skeletal muscle bioenergetics and proton efflux in migraine and cluster headache. J Neurol Sci. 1997 Feb;146(1):73-80. [CrossRef] [PubMed]
Lodi R, Montagna P, Soriani S, Iotti S, Arnaldi C, Cortelli P, et al. Deficit of brain and skeletal muscle bioenergetics and low brain magnesium in juvenile migraine: an in vivo 31P magnetic resonance spectro-scopy interictal study. Pediatr Res. 1997 Dec;42(6): 866-71. [CrossRef] [PubMed]
Luyten PR, den Hollander JA. Observation of metabo-lites in the human brain by MR spectroscopy. Radio-logy. 1986 Dec;161(3):795-8. [CrossRef] [PubMed]
Macrì MA, Garreffa G, Giove F, Ambrosini A, Guardati M, Pierelli F, et al. Cerebellar metabolite alterations detected in vivo by proton MR spectroscopy. Magn Reson Imaging. 2003 Dec;21(10):1201-6. [CrossRef] [PubMed]
Magistretti PJ, Pellerin L. Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. Philos Trans R Soc London Ser B, Biol Sci. 1999 Jul;354(1387):1155-63. [CrossRef] [PubMed]
Mancuso M, Orsucci D, Angelini C, Bertini E, Carelli V, Comi G Pietro, et al. The m.3243A>G mitochondrial DNA mutation and related phenotypes. A matter of gender? J Neurol. 2014 Mar;261(3):504-10. [CrossRef] [PubMed]
Mann EO, Paulsen O. Role of GABAergic inhibition in hippocampal network oscillations. Trends Neurosci. 2007 Jul;30(7):343-9. [CrossRef] [PubMed]
Mathew NT. Pathophysiology of chronic migraine and mode of action of preventive medications. Headache. 2011;51 Suppl 2:84-92. [CrossRef] [PubMed]
Miller BL. A review of chemical issues in 1H NMR spectroscopy: N-acetyl-L-aspartate, creatine and cho-line. NMR Biomed. 1991 Apr;4(2):47-52. [CrossRef] [PubMed]
Mohamed RE, Aboelsafa AA, Al-Malt AM. Interictal alterations of thalamic metabolic concentration ratios in migraine without aura detected by proton magnetic resonance spectroscopy. Egypt J Radiol Nucl Med. 2013;44(4):859-70. [CrossRef]
Montagna P, Cortelli P, Barbiroli B. Magnetic resonance spectroscopy studies in migraine. Cephalalgia. 1994 Jun;14(3):184-93. [CrossRef] [PubMed]
Montagna P, Cortelli P, Monari L, Pierangeli G, Parchi P, Lodi R, et al. 31P-magnetic resonance spectroscopy in migraine without aura. Neurology. 1994 Apr;44(4): 666-9. [CrossRef] [PubMed]
Niddam DM, Lai KL, Tsai SY, Lin YR, Chen WT, Fuh JL, et al. Neurochemical changes in the medial wall of the brain in chronic migraine. Brain. 2018;141(2): 377-90. [CrossRef] [PubMed]
Nioka S, Chance B, Hilberman M, Subramanian H V, Leigh JSJ, Veech RL, et al. Relationship between intracellular pH and energy metabolism in dog brain as measured by 31P-NMR. J Appl Physiol. 1987 May; 62(5):2094-102. [CrossRef] [PubMed]
Noseda R, Burstein R. Migraine pathophysiology: ana-tomy of the trigeminovascular pathway and associated neurological symptoms, cortical spreading depression, sensitization, and modulation of pain. Pain. 2013 Dec; 154 Suppl:S44-53. [CrossRef] [PubMed]
Oshinsky ML, Sanghvi MM, Maxwell CR, Gonzalez D, Spangenberg RJ, Cooper M, et al. Spontaneous trige-minal allodynia in rats: a model of primary headache. Headache. 2012 Oct;52(9):1336-49. [CrossRef] [PubMed]
Palmer AM, Marion DW, Botscheller ML, Bowen DM, DeKosky ST. Increased transmitter amino acid con-centration in human ventricular CSF after brain trauma. Neuroreport. 1994 Dec;6(1):153-6. [CrossRef] [PubMed]
Pearl PL, Hartka TR, Cabalza JL, Taylor J, Gibson MK. Inherited disorders of GABA metabolism. Future Neurol. 2006 Sep;1(5):631-6. [CrossRef] [PubMed]
Peek AL, Rebbeck T, Puts NA, Watson J, Aguila MER, Leaver AM. Brain GABA and glutamate levels across pain conditions: A systematic literature review and meta-analysis of 1H-MRS studies using the MRS-Q quality assessment tool. Neuroimage. 2020; 210 (January):116532. [CrossRef] [PubMed]
Petroff OA, Prichard JW, Behar KL, Alger JR, den Hollander JA, Shulman RG. Cerebral intracellular pH by 31P nuclear magnetic resonance spectroscopy. Neurology. 1985 Jun;35(6):781-8. [CrossRef] [PubMed]
Prescot A, Becerra L, Pendse G, Tully S, Jensen E, Hargreaves R, et al. Excitatory neurotransmitters in brain regions in interictal migraine patients. Mol Pain. 2009 Jun;5:34. [CrossRef] [PubMed]
Prescot A, Becerra L, Pendse G, Tully S, Jensen E, Hargreaves R, et al. Excitatory neurotransmitters in brain regions in interictal migraine patients. Mol Pain. 2009;5:1-11. [CrossRef] [PubMed]
Puts NAJ, Edden RAE. In vivo magnetic resonance spectroscopy of GABA: A methodological review. Prog Nucl Magn Reson Spectrosc. 2012;60:29-41. [CrossRef] [PubMed]
Rae CD. A guide to the metabolic pathways and function of metabolites observed in human brain 1H magnetic resonance spectra. Neurochem Res. 2014 Jan;39(1):1-36. [CrossRef] [PubMed]
Ramadan NM, Halvorson H, Vande-Linde A, Levine SR, Helpern JA, Welch KM. Low brain magnesium in migraine. Headache. 1989 Oct;29(9):590-3. [CrossRef] [PubMed]
Reyngoudt H, Achten E, Paemeleire K. Magnetic reso-nance spectroscopy in migraine: what have we learned so far? Cephalalgia. 2012 Aug;32(11):845-59. [CrossRef] [PubMed]
Reyngoudt H, De Deene Y, Descamps B, Paemeleire K, Achten E. (1)H-MRS of brain metabolites in mig-raine without aura: absolute quantification using the phantom replacement technique. MAGMA. 2010 Sep; 23(4):227-41. [CrossRef] [PubMed]
Reyngoudt H, Paemeleire K, Descamps B, De Deene Y, Achten E. 31P-MRS demonstrates a reduction in high-energy phosphates in the occipital lobe of mig-raine without aura patients. Cephalalgia. 2011 Sep; 31(12):1243-53. [CrossRef] [PubMed]
Reyngoudt H, Paemeleire K, Dierickx A, Descamps B, Vandemaele P, De Deene Y, et al. Does visual cortex lactate increase following photic stimulation in mig-raine without aura patients? A functional 1H-MRS study. J Headache Pain. 2011;12(3):295-302. [CrossRef] [PubMed]
Sangiorgi S, Mochi M, Riva R, Cortelli P, Monari L, Pierangeli G, et al. Abnormal platelet mitochondrial function in patients affected by migraine with and without aura. Cephalalgia. 1994 Feb;14(1):21-3. [CrossRef] [PubMed]
Sappey-Marinier D, Calabrese G, Fein G, Hugg JW, Biggins C, Weiner MW. Effect of photic stimulation on human visual cortex lactate and phosphates using 1H and 31P magnetic resonance spectroscopy. J Cereb blood flow Metab Off J Int Soc Cereb Blood Flow Metab. 1992 Jul;12(4):584-92. [CrossRef] [PubMed]
Sarchielli P, Tarducci R, Presciutti O, Gobbi G, Pelliccioli GP, Stipa G, et al. Functional 1H-MRS findings in migraine patients with and without aura assessed interictally. Neuroimage. 2005 Feb;24(4):1025-31. [CrossRef] [PubMed]
Schoenen J, Jacquy J, Lenaerts M. Effectiveness of high-dose riboflavin in migraine prophylaxis. A ran-domized controlled trial. Neurology. 1998 Feb;50(2): 466-70. [CrossRef] [PubMed]
Schubert F, Gallinat J, Seifert F, Rinneberg H. Gluta-mate concentrations in human brain using single voxel proton magnetic resonance spectroscopy at 3 Tesla. Neuroimage. 2004 Apr;21(4):1762-71. [CrossRef] [PubMed]
Schulz UG, Blamire AM, Corkill RG, Davies P, Styles P, Rothwell PM. Association between cortical metabolite levels and clinical manifestations of migrainous aura: an MR-spectroscopy study. Brain. 2007 Dec; 130(Pt 12):3102-10. [CrossRef] [PubMed]
Siniatchkin M, Sendacki M, Moeller F, Wolff S, Jansen O, Siebner H, et al. Abnormal changes of synaptic excitability in migraine with aura. Cereb Cortex. 2012 Oct;22(10):2207-16. [CrossRef] [PubMed]
Stærmose TG, Knudsen MK, Kasch H, Blicher JU. Cortical GABA in migraine with aura -an ultrashort echo magnetic resonance spectroscopy study. J Headache Pain. 2019;20(1). [CrossRef] [PubMed]
Sándor PS, Di Clemente L, Coppola G, Saenger U, Fumal A, Magis D, et al. Efficacy of coenzyme Q10 in migraine prophylaxis: a randomized controlled trial. Neurology. 2005 Feb;64(4):713-5. [CrossRef] [PubMed]
Sándor PS, Dydak U, Schoenen J, Kollias SS, Hess K, Boesiger P, et al. MR-spectroscopic imaging during visual stimulation in subgroups of migraine with aura. Cephalalgia. 2005 Jul;25(7):507-18. [CrossRef] [PubMed]
Uncini A, Lodi R, Di Muzio A, Silvestri G, Servidei S, Lugaresi A, et al. Abnormal brain and muscle energy metabolism shown by 31P-MRS in familial hemiplegic migraine. J Neurol Sci. 1995 Apr;129(2):214-22. [CrossRef] [PubMed]
van Dongen RM, Zielman R, Noga M, Dekkers OM, Hankemeier T, van den Maagdenberg AM, et al. Mig-raine biomarkers in cerebrospinal fluid: A systematic review and meta-analysis. Cephalalgia. 2017 Jan; 37(1):49-63. [CrossRef] [PubMed]
Vecchia D, Pietrobon D. Migraine: a disorder of brain excitatory-inhibitory balance? Trends Neurosci. 2012 Aug;35(8):507-20. [CrossRef] [PubMed]
Veech RL, Lawson JW, Cornell NW, Krebs HA. Cyto-solic phosphorylation potential. J Biol Chem. 1979 Jul; 254(14):6538-47. [CrossRef] [PubMed]
Wang S-J, Lirng J-F, Fuh J-L, Chen J-J. Reduction in hypothalamic 1H-MRS metabolite ratios in patients with cluster headache. J Neurol Neurosurg Psychiatry. 2006 May;77(5):622-5. [CrossRef] [PubMed]
Watanabe H, Kuwabara T, Ohkubo M, Tsuji S, Yuasa T. Elevation of cerebral lactate detected by localized 1H-magnetic resonance spectroscopy in migraine during the interictal period. Neurology. 1996 Oct; 47(4):1093-5. [CrossRef] [PubMed]
Welch KM, Levine SR, D’Andrea G, Helpern JA. Brain pH in migraine: an in vivo phosphorus-31 magnetic resonance spectroscopy study. Cephalalgia. 1988 Dec; 8(4):273-7. [CrossRef] [PubMed]
Welch KM, Levine SR, D’Andrea G, Schultz LR, Helpern JA. Preliminary observations on brain energy metabolism in migraine studied by in vivo phosphorus 31 NMR spectroscopy. Neurology. 1989 Apr;39(4): 538-41. [CrossRef] [PubMed]
Welch KM, Ramadan NM. Mitochondria, magnesium and migraine. J Neurol Sci. 1995 Dec;134(1-2):9-14. [CrossRef] [PubMed]
Younis S, Hougaard A, Vestergaard MB, Larsson HBW, Ashina M. Migraine and magnetic resonance spectro-scopy: A systematic review. Curr Opin Neurol. 2017; 30(3):246-62. [CrossRef] [PubMed]
Zielman R, Teeuwisse WM, Bakels F, Van der Grond J, Webb A, van Buchem MA, et al. Biochemical changes in the brain of hemiplegic migraine patients measured with 7 tesla 1H-MRS. Cephalalgia. 2014 Oct;34(12): 959-67. [CrossRef] [PubMed]