[en] Increasing evidence points towards the role of mitochondrial functioning, energy metabolism, and oxidative stress in migraine. However not all previous research has been conclusive and some mitochondrial function/oxidative stress markers have not yet been examined. To this end, alpha-lipoic acid (ALA), total thiols, total plasma antioxidant capacity (TAC), lipid peroxide (PerOx), oxidised LDL (oxLDL), HbA1c and lactate were determined in the serum of 32 higher frequency episodic migraineurs (5-14 migraine days/ months, 19 with aura, 28 females) in this cross-sectional study. The majority of patients had abnormally low ALA and lactate levels (87.5% and 78.1%, respectively). 46.9% of the patients had abnormally high PerOx values, while for thiols and TAC over one third of patients had abnormally low values (31.2% and 37.5%, respectively). 21.9% of patients had abnormally low HbA1c and none had an HbA1c level above 5.6%. oxLDL was normal in all but one patient. This study provides further evidence for a role of oxidative stress and altered metabolism in migraine pathophysiology, which might represent a suitable therapeutic target. ALA, being too low in almost 90% of patients, might represent a potential biomarker for migraine. Further research is needed to replicate these results, in particular a comparison with a control group.This study is part of the trial registration: ClinicalTrials.gov: NCT03132233, registered on 27.04.2017, https://clinicaltrials.gov/ct2/show/NCT03132233 .
Disciplines :
Neurology
Author, co-author :
Gross, Elena C; Division of Paediatric Neurology, University Children's Hospital Basel (UKBB), University of Basel, Basel, Switzerland. elena.gross@oxfordalumni.org
Putananickal, Niveditha; Division of Paediatric Neurology, University Children's Hospital Basel (UKBB), University of Basel, Basel, Switzerland
Orsini, Anna-Lena; Division of Paediatric Neurology, University Children's Hospital Basel (UKBB), University of Basel, Basel, Switzerland ; Neurology Department, University Hospital Basel (USB), University of Basel, Basel, Switzerland
Vogt, Deborah R; Clinical Trail Unit (CTU), Department of Clinical Research, University Hospital Basel (USB), University of Basel, Basel, Switzerland
Sandor, Peter S; RehaClinic Group, Bad Zurzach, University of Zurich, Zurich, Switzerland ; University of Zurich, Zurich, Switzerland
Schoenen, Jean ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
Fischer, Dirk; Division of Paediatric Neurology, University Children's Hospital Basel (UKBB), University of Basel, Basel, Switzerland
Language :
English
Title :
Mitochondrial function and oxidative stress markers in higher-frequency episodic migraine.
Stovner, L. J., Hoff, J. M., Svalheim, S. & Gilhus, N. E. Neurological disorders in the Global Burden of Disease 2010 study. Acta Neurol. Scand. 129(198), 1–6 (2014). DOI: 10.1111/ane.12229
Gray, P. A. & Burtness, H. I. Hypoglycemic headache*. Endocrinology 19(5), 549–560 (1935). DOI: 10.1210/endo-19-5-549
Barbiroli, B. et al. Abnormal brain and muscle energy metabolism shown by 31P magnetic resonance spectroscopy in patients affected by migraine with aura. Neurology 42(6), 1209–1214 (1992). DOI: 10.1212/WNL.42.6.1209
Kim, J. H. et al. Interictal metabolic changes in episodic migraine: A voxel-based FDG-PET study. Cephalalgia 30(1), 53–61 (2010). DOI: 10.1111/j.1468-2982.2009.01890.x
Lodi, R. et al. Deficit of brain and skeletal muscle bioenergetics and low brain magnesium in juvenile migraine: An in vivo 31P magnetic resonance spectroscopy interictal study. Pediatr. Res. 42(6), 866–871 (1997). DOI: 10.1203/00006450-199712000-00024
Lodi, R. et al. Deficient energy metabolism is associated with low free magnesium in the brains of patients with migraine and cluster headache. Brain Res. Bull. 54(4), 437–441 (2001). DOI: 10.1016/S0361-9230(01)00440-3
Montagna, P. et al. 31P-magnetic resonance spectroscopy in migraine without aura. Neurology 44(4), 666–669 (1994). DOI: 10.1212/WNL.44.4.666
Reyngoudt, H., Achten, E. & Paemeleire, K. Magnetic resonance spectroscopy in migraine: What have we learned so far?. Cephalalgia Int. J. Headache 32(11), 845–859 (2012). DOI: 10.1177/0333102412452048
Schulz, U. G. et al. Association between cortical metabolite levels and clinical manifestations of migrainous aura: An MR-spectroscopy study. Brain 130(Pt 12), 3102–3110 (2007). DOI: 10.1093/brain/awm165
Welch, K. M., Levine, S. R., D’Andrea, G., Schultz, L. R. & Helpern, J. A. Preliminary observations on brain energy metabolism in migraine studied by in vivo phosphorus 31 NMR spectroscopy. Neurology 39(4), 538–541 (1989). DOI: 10.1212/WNL.39.4.538
Lodi, R. et al. Quantitative analysis of skeletal muscle bioenergetics and proton efflux in migraine and cluster headache. J. Neurol. Sci. 146(1), 73–80 (1997). DOI: 10.1016/S0022-510X(96)00287-0
Barbiroli, B. et al. Complicated migraine studied by phosphorus magnetic resonance spectroscopy. Cephalalgia 10(5), 263–272 (1990). DOI: 10.1046/j.1468-2982.1990.1005263.x
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 migraine without aura patients. Cephalalgia Int. J. Headache 31(12), 1243–1253 (2011). DOI: 10.1177/0333102410394675
Hockaday Judith, M., Williamson, D. H. & Whitty, C. W. M. Blood-glucose levels and fatty-acid metabolism in migraine related to fasting. Lancet 297(7710), 1153–1156 (1971). DOI: 10.1016/S0140-6736(71)91662-X
Shaw, S. W., Johnson, R. H. & Keogh, H. J. Metabolic changes during glucose tolerance tests in migraine attacks. J. Neurol. Sci. 33(1–2), 51–59 (1977). DOI: 10.1016/0022-510X(77)90181-2
Dexter, J. D., Roberts, J. & Byer, J. A. The five hour glucose tolerance test and effect of low sucrose diet in migraine. Headache J. Head Face Pain 18(2), 91–94 (1978). DOI: 10.1111/j.1526-4610.1978.hed1802091.x
Wang, X. et al. Are glucose and insulin metabolism and diabetes associated with migraine? A community-based, case-control study. J. Oral Facial Pain Headache 31(3), 240–250 (2017). DOI: 10.11607/ofph.1843
Rainero, I. et al. Insulin sensitivity is impaired in patients with migraine. Cephalalgia 25(8), 593–597 (2005). DOI: 10.1111/j.1468-2982.2005.00928.x
Fava, A. et al. Chronic migraine in women is associated with insulin resistance: A cross-sectional study. Eur. J. Neurol. Off. J. Eur. Fed. Neurol. Soc. 21(2), 267–272 (2014).
Cavestro, C. et al. Insulin metabolism is altered in migraineurs: A new pathogenic mechanism for migraine?. Headache J. Head Face Pain 47(10), 1436–1442 (2007). DOI: 10.1111/j.1526-4610.2007.00719.x
Shaik, M. M. & Gan, S. H. Vitamin supplementation as possible prophylactic treatment against migraine with aura and menstrual migraine. Biomed. Res. Int. 2015, 469529 (2015).
Boehnke, C. et al. High-dose riboflavin treatment is efficacious in migraine prophylaxis: An open study in a tertiary care centre. Eur. J. Neurol. 11(7), 475–477 (2004). DOI: 10.1111/j.1468-1331.2004.00813.x
Condò, M., Posar, A., Arbizzani, A. & Parmeggiani, A. Riboflavin prophylaxis in pediatric and adolescent migraine. J. Headache Pain 10(5), 361–365 (2009). DOI: 10.1007/s10194-009-0142-2
Gaul, C., Diener, H.-C. & Danesch, U. Migravent® Study Group on behalf of the MS. Improvement of migraine symptoms with a proprietary supplement containing riboflavin, magnesium and Q10: A randomized, placebo-controlled, double-blind, multicenter trial. J. Headache Pain 16, 516 (2015). DOI: 10.1186/s10194-015-0516-6
Schoenen, J., Jacquy, J. & Lenaerts, M. Effectiveness of high-dose riboflavin in migraine prophylaxis. A randomized controlled trial. Neurology 50(2), 466–470 (1998). DOI: 10.1212/WNL.50.2.466
Rahimdel, A., Mellat, A., Zeinali, A., Jafari, E. & Ayatollahi, P. Comparison between intravenous sodium valproate and subcutaneous sumatriptan for treatment of acute migraine attacks; double-blind randomized clinical trial. Iran. J. Med. Sci. 39(2 Suppl), 171–177 (2014).
Thompson, D. F. & Saluja, H. S. Prophylaxis of migraine headaches with riboflavin: A systematic review. J. Clin. Pharm. Ther. 42(4), 394–403 (2017). DOI: 10.1111/jcpt.12548
Di Lorenzo, C. et al. Mitochondrial DNA haplogroups influence the therapeutic response to riboflavin in migraineurs. Neurology 72(18), 1588–1594 (2009). DOI: 10.1212/WNL.0b013e3181a41269
Dahri, M., Hashemilar, M., Asghari-Jafarabadi, M. & Tarighat-Esfanjani, A. Efficacy of coenzyme Q10 for the prevention of migraine in women: A randomized, double-blind, placebo-controlled study. Eur. J. Integr. Med. 16, 8–14 (2017). DOI: 10.1016/j.eujim.2017.10.003
Dahri, M., Tarighat-Esfanjani, A., Asghari-Jafarabadi, M. & Hashemilar, M. Oral coenzyme Q10 supplementation in patients with migraine: Effects on clinical features and inflammatory markers. Nutr. Neurosci. 1, 1–9 (2018). DOI: 10.3934/Neuroscience.2018.1.1
Sándor, P. S. et al. Efficacy of coenzyme Q10 in migraine prophylaxis: A randomized controlled trial. Neurology 64(4), 713–715 (2005). DOI: 10.1212/01.WNL.0000151975.03598.ED
Hajihashemi, P., Askari, G., Khorvash, F., Reza Maracy, M. & Nourian, M. The effects of concurrent Coenzyme Q10, L-carnitine supplementation in migraine prophylaxis: A randomized, placebo-controlled, double-blind trial. Cephalalgia 6, 0333102418821661 (2019).
Shoeibi, A. et al. Effectiveness of coenzyme Q10 in prophylactic treatment of migraine headache: An open-label, add-on, controlled trial. Acta Neurol. Belg. 117(1), 103–109 (2017). DOI: 10.1007/s13760-016-0697-z
Rozen, T. et al. Open label trial of coenzyme Q10 as a migraine preventive. Cephalalgia 22(2), 137–141 (2002). DOI: 10.1046/j.1468-2982.2002.00335.x
Chiu, H.-Y., Yeh, T.-H., Huang, Y.-C. & Chen, P.-Y. Effects of intravenous and oral magnesium on reducing migraine: A meta-analysis of randomized controlled trials. Pain Physician 19(1), E97-112 (2016).
Magis, D. et al. A randomized double-blind placebo-controlled trial of thioctic acid in migraine prophylaxis. Headache 47(1), 52–57 (2007). DOI: 10.1111/j.1526-4610.2006.00626.x
Cavestro, C. et al. Alpha-lipoic acid shows promise to improve migraine in patients with insulin resistance: A 6-month exploratory study. J. Med. Food 21(3), 269–273 (2018). DOI: 10.1089/jmf.2017.0068
Ali, A. M., Awad, T. G. & Al-Adl, N. M. Efficacy of combined topiramate/thioctic acid therapy in migraine prophylaxis. Saudi Pharm. J. 18(4), 239–243 (2010). DOI: 10.1016/j.jsps.2010.07.006
Strahlman, R. S. Can ketosis help migraine sufferers? A case report. Headache 46(1), 182 (2006). DOI: 10.1111/j.1526-4610.2006.00321_5.x
Di Lorenzo, C. et al. Diet transiently improves migraine in two twin sisters: Possible role of ketogenesis?. Funct. Neurol. 28(4), 305–308 (2013).
Maggioni, F., Margoni, M. & Zanchin, G. Ketogenic diet in migraine treatment: A brief but ancient history. Cephalalgia Int. J. Headache 31(10), 1150–1151 (2011). DOI: 10.1177/0333102411412089
Schnabel, T. G. An experience with a ketogenic dietary in migraine. Ann. Intern. Med. 2(4), 341 (1928). DOI: 10.7326/0003-4819-2-4-341
Di Lorenzo, C. et al. Migraine improvement during short lasting ketogenesis: A proof-of-concept study. Eur. J. Neurol. Off. J. Eur. Fed. Neurol. Soc. 22(1), 170–177 (2014).
Di Lorenzo, C. et al. Cortical functional correlates of responsiveness to short-lasting preventive intervention with ketogenic diet in migraine: A multimodal evoked potentials study. J. Headache Pain 17(1), 58 (2016). DOI: 10.1186/s10194-016-0650-9
Gross, E. C., Klement, R. J., Schoenen, J., D’Agostino, D. P. & Fischer, D. Potential protective mechanisms of ketone bodies in migraine prevention. Nutrients 11(4), 811 (2019). DOI: 10.3390/nu11040811
Montagna, P. et al. Mitochondrial abnormalities in migraine. Preliminary findings. Headache J. Head Face Pain 28(7), 477–480 (1988). DOI: 10.1111/j.1526-4610.1988.hed2807477.x
Okada, H., Araga, S., Takeshima, T. & Nakashima, K. Plasma lactic acid and pyruvic acid levels in migraine and tension-type headache. Headache 38(1), 39–42 (1998). DOI: 10.1046/j.1526-4610.1998.3801039.x
Birben, E., Sahiner, U. M., Sackesen, C., Erzurum, S. & Kalayci, O. Oxidative stress and antioxidant defense. World Allergy Organ. J. 5(1), 9 (2012). DOI: 10.1097/WOX.0b013e3182439613
Ogino, K. & Wang, D.-H. Biomarkers of oxidative/nitrosative stress: An approach to disease prevention. Acta Med. Okayama 61(4), 181–189 (2007).
Sies, H. Oxidative stress: A concept in redox biology and medicine. Redox Biol. 4, 180–183 (2015). DOI: 10.1016/j.redox.2015.01.002
Borkum, J. M. Migraine triggers and oxidative stress: A narrative review and synthesis. Headache 56(1), 12–35 (2015). DOI: 10.1111/head.12725
Gross, E. C., Lisicki, M., Fischer, D., Sandor, P. S. & Schoenen, J. The metabilic face of migraine. Nat. Neurol. 15(11), 627–643 (2019). DOI: 10.1038/s41582-019-0255-4
Benemei, S., Fusi, C., Trevisan, G. & Geppetti, P. The TRPA1 channel in migraine mechanism and treatment. Br. J. Pharmacol. 171(10), 2552–2567 (2014). DOI: 10.1111/bph.12512
Kozai, D., Ogawa, N. & Mori, Y. Redox regulation of transient receptor potential channels. Antioxid. Redox Signal. 21(6), 971–986 (2014). DOI: 10.1089/ars.2013.5616
Alp, R., Selek, S., Alp, S. I., Taşkin, A. & Koçyiğit, A. Oxidative and antioxidative balance in patients of migraine. Eur. Rev. Med. Pharmacol. Sci. 14(10), 877–882 (2010).
Aytaç, B. et al. Decreased antioxidant status in migraine patients with brain white matter hyperintensities. Neurol. Sci. 35(12), 1925–1929 (2014). DOI: 10.1007/s10072-014-1864-8
Bernecker, C. et al. Oxidative stress is associated with migraine and migraine-related metabolic risk in females. Eur. J. Neurol. 18(10), 1233–1239 (2011). DOI: 10.1111/j.1468-1331.2011.03414.x
Bolayir, E. et al. Intraerythrocyte antioxidant enzyme activities in migraine and tension-type headaches. J. Chin. Med. Assoc. 67(6), 263–267 (2004).
Ciancarelli, I., Tozzi-Ciancarelli, M., Massimo, C. D., Marini, C. & Carolei, A. Urinary nitric oxide metabolites and lipid peroxidation by-products in migraine. Cephalalgia 23(1), 39–42 (2003). DOI: 10.1046/j.1468-2982.2003.00447.x
Ciancarelli, I., Tozzi-Ciancarelli, M., Spacca, G., Massimo, C. D. & Carolei, A. Relationship between biofeedback and oxidative stress in patients with chronic migraine. Cephalalgia 27(10), 1136–1141 (2007). DOI: 10.1111/j.1468-2982.2007.01398.x
Eren, Y., Dirik, E., Neşelioğlu, S. & Erel, Ö. Oxidative stress and decreased thiol level in patients with migraine: Cross-sectional study. Acta Neurol. Belg. 115(4), 643–649 (2015). DOI: 10.1007/s13760-015-0427-y
Geyik, S., Altunısık, E., Neyal, A. M. & Taysi, S. Oxidative stress and DNA damage in patients with migraine. J. Headache Pain 17(1), 10 (2016). DOI: 10.1186/s10194-016-0606-0
Gumusyayla, S. et al. A novel oxidative stress marker in migraine patients: Dynamic thiol-disulphide homeostasis. Neurol. Sci. Off. J. Ital. Neurol. Soc. Ital. Soc. Clin. Neurophysiol. 37(8), 1311–1317 (2016).
Shimomura, T. et al. Platelet superoxide dismutase in migraine and tension-type headache. Cephalalgia 14(3), 215–218 (1994). DOI: 10.1046/j.1468-2982.1994.014003215.x
Tozzi-Ciancarelli, M. et al. Oxidative stress and platelet responsiveness in migraine. Cephalalgia 17(5), 580–584 (1997). DOI: 10.1046/j.1468-2982.1997.1705580.x
Tripathi, G. M., Kalita, J. & Misra, U. K. A study of oxidative stress in migraine with special reference to prophylactic therapy. Int. J. Neurosci. 128(4), 318–324 (2018). DOI: 10.1080/00207454.2017.1374959
Tuncel, D., Tolun, F. I., Gokce, M., İmrek, S. & Ekerbiçer, H. Oxidative stress in migraine with and without aura. Biol. Trace Elem. Res. 126(1–3), 92–97 (2008). DOI: 10.1007/s12011-008-8193-9
Yilmaz, G., Sürer, H., Inan, L. E., Coskun, O. & Yücel, D. Increased nitrosative and oxidative stress in platelets of migraine patients. Tohoku J. Exp. Med. 211(1), 23–30 (2007). DOI: 10.1620/tjem.211.23
Neri, M. et al. A meta-analysis of biomarkers related to oxidative stress and nitric oxide pathway in migraine. Cephalalgia 35(10), 931–937 (2015). DOI: 10.1177/0333102414564888
Gross, E. et al. Efficacy and safety of exogenous ketone bodies for preventive treatment of migraine: A study protocol for a single-centred, randomised, placebo-controlled, double-blind crossover trial. Trials 20(1), 61 (2019). DOI: 10.1186/s13063-018-3120-7
Headache Classification Committee of the International Headache Society (IHS). The International Classification of Headache Disorders, 3rd edition (beta version). Cephalalgia Int. J. Headache 33(9), 629–808 (2013). DOI: 10.1177/0333102413485658
Benz, T. et al. Translation, cross-cultural adaptation and reliability of the German version of the migraine disability assessment (MIDAS) questionnaire. Health Qual. Life Outcomes 16(1), 42 (2018). DOI: 10.1186/s12955-018-0871-5
Stepan, H., Heihoff-Klose, A. & Faber, R. Reduced antioxidant capacity in second-trimester pregnancies with pathological uterine perfusion. Ultrasound Obstet. Gynecol. 23(6), 579–583 (2004). DOI: 10.1002/uog.1045
Hildebrandt, W., Alexander, S., Bärtsch, P. & Dröge, W. Effect of N-acetyl-cysteine on the hypoxic ventilatory response and erythropoietin production: Linkage between plasma thiol redox state and O(2) chemosensitivity. Blood 99(5), 1552–1555 (2002). DOI: 10.1182/blood.V99.5.1552
Koubaa, N. et al. Hyperhomocysteinemia and elevated ox-LDL in Tunisian type 2 diabetic patients: Role of genetic and dietary factors. Clin. Biochem. 40(13), 1007–1014 (2007). DOI: 10.1016/j.clinbiochem.2007.05.017
Banne, A. F., Amiri, A. & Pero, R. W. Reduced level of serum thiols in patients with a diagnosis of active disease. J. Anti-Aging Med. 6(4), 327–334 (2003). DOI: 10.1089/109454503323028920
Wasserstein, R. L., Schirm, A. L. & Lazar, N. A. Moving to a world beyond “p < 0.05”. Am. Stat. 73(1), 1–19 (2019). DOI: 10.1080/00031305.2019.1583913
Team RC. R Foundation for Statistical Computing; Vienna, Austria: 2014. R: A language and environment for statistical computing. 2018;2013.
Bast, A. & Haenen, G. R. M. M. Lipoic acid: A multifunctional antioxidant. BioFactors 17(1–4), 207–213 (2003). DOI: 10.1002/biof.5520170120
Packer, L., Witt, E. H. & Tritschler, H. J. alpha-Lipoic acid as a biological antioxidant. Free Radic. Biol. Med. 19(2), 227–250 (1995). DOI: 10.1016/0891-5849(95)00017-R
Müller, U. & Krieglstein, J. Prolonged pretreatment with α-lipoic acid protects cultured neurons against hypoxic, glutamate-, or iron-induced injury. J. Cereb. Blood Flow Metab. 15(4), 624–630 (1995). DOI: 10.1038/jcbfm.1995.77
Kim, W.-J., Kang, J.-Y., Kwon, D.-K., Song, Y.-J. & Lee, K.-H. Effects of α-lipoic acid supplementation on malondialdehyde contents and superoxide dismutase in rat skeletal muscles. Food Sci. Biotechnol. 20(4), 1133 (2011). DOI: 10.1007/s10068-011-0154-y
Packer, L. alpha-Lipoic acid: A metabolic antioxidant which regulates NF-kappa B signal transduction and protects against oxidative injury. Drug Metab. Rev. 30(2), 245–275 (1998). DOI: 10.3109/03602539808996311
Packer, L., Roy, S. & Sen, C. K. Alpha-lipoic acid: A metabolic antioxidant and potential redox modulator of transcription. Adv. Pharmacol. 38, 79–101 (1997). DOI: 10.1016/S1054-3589(08)60980-1
Huerta, A. E., Navas-Carretero, S., Prieto-Hontoria, P. L., Martínez, J. A. & Moreno-Aliaga, M. J. Effects of α-lipoic acid and eicosapentaenoic acid in overweight and obese women during weight loss. Obesity 23(2), 313–321 (2015). DOI: 10.1002/oby.20966
Zhang, Y. et al. Amelioration of lipid abnormalities by α-lipoic acid through antioxidative and anti-inflammatory effects. Obesity 19(8), 1647–1653 (2011). DOI: 10.1038/oby.2011.121
Gupta, R., Pathak, R., Bhatia, M. S. & Banerjee, B. D. Comparison of oxidative stress among migraineurs, tension-type headache subjects, and a control group. Ann. Indian Acad. Neurol. 12(3), 167 (2009). DOI: 10.4103/0972-2327.56316
Cadenas, E. Biochemistry of oxygen toxicity. Annu. Rev. Biochem. 58(1), 79–110 (1989). DOI: 10.1146/annurev.bi.58.070189.000455
Pasaoglu, H., Sancak, B. & Bukan, N. Lipid peroxidation and resistance to oxidation in patients with type 2 diabetes mellitus. Tohoku J. Exp. Med. 203(3), 211–218 (2004). DOI: 10.1620/tjem.203.211
McBean, G. J., Aslan, M., Griffiths, H. R. & Torrão, R. C. Thiol redox homeostasis in neurodegenerative disease. Redox Biol. 22(5), 186–194 (2015). DOI: 10.1016/j.redox.2015.04.004
Sandor, P. S. et al. MR-spectroscopic imaging during visual stimulation in subgroups of migraine with aura. Cephalalgia 25(7), 507–518 (2005). DOI: 10.1111/j.1468-2982.2005.00900.x
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 47(4), 1093–1095 (1996). DOI: 10.1212/WNL.47.4.1093
Reyngoudt, H. et al. Does visual cortex lactate increase following photic stimulation in migraine without aura patients? A functional (1)H-MRS study. J. Headache Pain 12(3), 295–302 (2011). DOI: 10.1007/s10194-011-0295-7
Prescot, A. et al. Excitatory neurotransmitters in brain regions in interictal migraine patients. Mol. Pain 30(5), 34 (2009).
Mohamed, R. E., Aboelsafa, A. A. & Al-Malt, A. M. Interictal alterations of thalamic metabolic concentration ratios in migraine without aura detected by proton magnetic resonance spectroscopy. Egypt. J. Radiol. Nucl. Med. 44(4), 859–870 (2013). DOI: 10.1016/j.ejrnm.2013.08.004
Becerra, L. et al. A “complex” of brain metabolites distinguish altered chemistry in the cingulate cortex of episodic migraine patients. Neuroimage Clin. 11, 588–594 (2016). DOI: 10.1016/j.nicl.2016.03.020
Sappey-Marinier, D. et al. Effect of photic stimulation on human visual cortex lactate and phosphates using 1H and 31P magnetic resonance spectroscopy. J. Cereb. Blood Flow Metab. 12(4), 584–592 (1992). DOI: 10.1038/jcbfm.1992.82
Magistretti, P. J. & Pellerin, L. Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. Philos. Trans. R Soc. Lond. B Biol. Sci. 354(1387), 1155–1163 (1999). DOI: 10.1098/rstb.1999.0471
Gantenbein, A. R. et al. Sensory information processing may be neuroenergetically more demanding in migraine patients. NeuroReport 24(4), 202–205 (2013). DOI: 10.1097/WNR.0b013e32835eba81
Riske, L., Thomas, R. K., Baker, G. B. & Dursun, S. M. Lactate in the brain: An update on its relevance to brain energy, neurons, glia and panic disorder. Ther. Adv. Psychopharmacol. 7(2), 85 (2017). DOI: 10.1177/2045125316675579
Boumezbeur, F. et al. The contribution of blood lactate to brain energy metabolism in humans measured by dynamic 13C nuclear magnetic resonance spectroscopy. J. Neurosci. 30(42), 13983–13991 (2010). DOI: 10.1523/JNEUROSCI.2040-10.2010