Cortical functional correlates of responsiveness to short-lasting preventive intervention with ketogenic diet in migraine: a multimodal evoked potentials study

Journal of Headache and Pain

Volumn 17, Issue 1, 2016, Pages

  Di Lorenzo, Cherubino ^a   Coppola, Gianluca ^b   Bracaglia, Martina ^c   Di Lenola, Davide ^c   Evangelista, Maurizio ^d   Sirianni, Giulio ^e   Rossi, Paolo ^f   Di Lorenzo, Giorgio ^g   Serrao, Mariano ^c   Parisi, Vincenzo ^b   Pierelli, Francesco ^c,h  

^a IRCCS FONDAZIONE DON CARLO GNOCCHI   (Italy)

^b IRCCS FONDAZIONE BIETTI   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d CATHOLIC UNIVERSITY   (Italy)

^e Wellness and Dietary Medicine   (Italy)

^f INI   (Italy)

^g UNIVERSITY OF ROME TOR VERGATA   (Italy)

^h IRCCS NEUROMED   (Italy)

Author keywords

Diet; Habituation; Ketogenesis; Migraine; Somatosensory evoked potentials; Visual evoked potentials

Indexed keywords

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DIETETICS; ELECTRONEUROLOGY; EVOKED CORTICAL RESPONSE; FEMALE; HABITUATION; HUMAN; INTERVENTION STUDY; KETOGENESIS; KETOGENIC DIET; LINEAR REGRESSION ANALYSIS; MALE; MEDIAN NERVE; MIGRAINE; PREVENTION STUDY; PRIORITY JOURNAL; SOMATOSENSORY EVOKED POTENTIAL; VISUAL EVOKED POTENTIAL; AUDITORY EVOKED POTENTIAL; BRAIN CORTEX; DIET THERAPY; EVOKED RESPONSE; MIDDLE AGED; MIGRAINE DISORDERS; PATHOPHYSIOLOGY;

ADULT; CEREBRAL CORTEX; EVOKED POTENTIALS; EVOKED POTENTIALS, AUDITORY; EVOKED POTENTIALS, SOMATOSENSORY; EVOKED POTENTIALS, VISUAL; FEMALE; HABITUATION, PSYCHOPHYSIOLOGIC; HUMANS; KETOGENIC DIET; MALE; MIDDLE AGED; MIGRAINE DISORDERS;

EID: 84973897703     PISSN: 11292369     EISSN: 11292377     Source Type: Journal    
DOI: 10.1186/s10194-016-0650-9     Document Type: Article

References (50)

1. Rossi P, Di Lorenzo G, Malpezzi MG et al (2005) Prevalence, pattern and predictors of use of complementary and alternative medicine (CAM) in migraine patients attending a headache clinic in Italy. Cephalalgia 25:493–506
2. Rossi P, Torelli P, Di Lorenzo C et al (2008) Use of complementary and alternative medicine by patients with cluster headache: results of a multi-centre headache clinic survey. Complement Ther Med 16:220–227
3. Coppola G, Di Lorenzo C, Serrao M et al (2015) Pathophysiological targets for non-pharmacological treatment of migraine. Cephalalgia. doi:10.1177/0333102415620908
4. Bigal ME, Lipton RB (2006) Obesity is a risk factor for transformed migraine but not chronic tension-type headache. Neurology 67:252–257
5. Chai N, Scher AI, Moghekar A et al (2014) Obesity and headache: part I--a systematic review of the epidemiology of obesity and headache. Headache 54:219–234
6. Rainero I, Limone P, Ferrero M et al (2005) Insulin sensitivity is impaired in patients with migraine. Cephalalgia 25:593–597
7. Cavestro C, Rosatello A, Micca G et al (2007) Insulin metabolism is altered in migraineurs: a new pathogenic mechanism for migraine? Headache 47:1436–1442
8. Di Lorenzo C, Currà A, Sirianni G et al (2013) Diet transiently improves migraine in two twin sisters: possible role of ketogenesis? Funct Neurol 28:305–308
9. Di Lorenzo C, Coppola G, Sirianni G et al (2015) Migraine improvement during short lasting ketogenesis: a proof-of-concept study. Eur J Neurol 22:170–177
10. Cantello R, Varrasi C, Tarletti R et al (2007) Ketogenic diet: electrophysiological effects on the normal human cortex. Epilepsia 48:1756–1763
11. Blaise JH, Ruskin DN, Koranda JL, Masino SA (2015) Effects of a ketogenic diet on hippocampal plasticity in freely moving juvenile rats. Physiol Rep 3:e12411
12. Coppola G, Di Lorenzo C, Schoenen J, Pierelli F (2013) Habituation and sensitization in primary headaches. J Headache Pain 14:65
13. Magis D, Vigano A, Sava S et al (2013) Pearls and pitfalls: electrophysiology for primary headaches. Cephalalgia 33:526–539
14. Schoenen J (1996) Deficient habituation of evoked cortical potentials in migraine: a link between brain biology, behavior and trigeminovascular activation? Biomed Pharmacother = Biomédecine pharmacothérapie 50:71–78
15. McDonald, McDonald L (1998) The Ketogenic Diet. Austin, Texas: Lyle McDonald
16. Coppola G, Bracaglia M, Di Lenola D et al (2015) Visual evoked potentials in subgroups of migraine with aura patients. J Headache Pain 16:92
17. Ozkul Y, Uckardes A (2002) Median nerve somatosensory evoked potentials in migraine. Eur J Neurol 9:227–232
18. Coppola G, Iacovelli E, Bracaglia M et al (2013) Electrophysiological correlates of episodic migraine chronification: evidence for thalamic involvement. J Headache Pain 14:76
19. Coppola G, Currà A, Di Lorenzo C et al (2010) Abnormal cortical responses to somatosensory stimulation in medication-overuse headache. BMC Neurol 10:126
20. Coppola G, Parisi V, Di Lorenzo C et al (2013) Lateral inhibition in visual cortex of migraine patients between attacks. J Headache Pain 14:20
21. Harris JD (1943) Habituatory response decrement in the intact organism. Psychol Bull 40:385–422
22. Di Lorenzo C, Coppola G, Currà A et al (2012) Cortical response to somatosensory stimulation in medication overuse headache patients is influenced by angiotensin converting enzyme (ACE) I/D genetic polymorphism. Cephalalgia 32:1189–1197
23. Di Lorenzo C, Di Lorenzo G, Daverio A et al (2012) The Val66Met polymorphism of the BDNF gene influences trigeminal pain-related evoked responses. J Pain 13:866–873
24. Di Lorenzo C, Daverio A, Pasqualetti P et al (2014) The upstream Variable Number Tandem Repeat polymorphism of the monoamine oxidase type A gene influences trigeminal pain-related evoked responses. Eur J Neurosci 39:501–507
25. Koranda JL, Ruskin DN, Masino SA, Blaise JH (2011) A ketogenic diet reduces long-term potentiation in the dentate gyrus of freely behaving rats. J Neurophysiol 106:662–666
26. Groves PM, Thompson RF (1970) Habituation: a dual-process theory. Psychol Rev 77:419–450
27. Wheless JW (2008) History of the ketogenic diet. Epilepsia 8:3–5
28. Klein P, Tyrlikova I, Mathews GC (2014) Dietary treatment in adults with refractory epilepsy: a review. Neurology 83:1978–1985
29. Stafstrom CE, Wang C, Jensen FE (1999) Electrophysiological observations in hippocampal slices from rats treated with the ketogenic diet. Dev Neurosci 21:393–399
30. Bough KJ, Schwartzkroin PA, Rho JM (2003) Calorie restriction and ketogenic diet diminish neuronal excitability in rat dentate gyrus in vivo. Epilepsia 44:752–760
31. Kawamura M, Ruskin DN, Geiger JD et al (2014) Ketogenic diet sensitizes glucose control of hippocampal excitability. J Lipid Res 55:2254–2260
32. Nylen K, Velazquez JL, Likhodii SS et al (2008) A ketogenic diet rescues the murine succinic semialdehyde dehydrogenase deficient phenotype. Exp Neurol 210:449–457
33. Simeone TA, Samson KK, Matthews SA, Simeone KA (2014) In vivo ketogenic diet treatment attenuates pathologic sharp waves and high frequency oscillations in in vitro hippocampal slices from epileptic Kv 1.1α knockout mice. Epilepsia 55:e44–e49
34. Erecińska M, Nelson D, Daikhin Y, Yudkoff M (1996) Regulation of GABA level in rat brain synaptosomes: fluxes through enzymes of the GABA shunt and effects of glutamate, calcium, and ketone bodies. J Neurochem 67:2325–2334
35. Sato K, Kashiwaya Y, Keon CA et al (1995) Insulin, ketone bodies, and mitochondrial energy transduction. FASEB J 9:651–658
36. Coppola G, Pierelli F, Schoenen J (2007) Is the cerebral cortex hyperexcitable or hyperresponsive in migraine? Cephalalgia 27:1427–1439
37. Coppola G, Bracaglia M, Di Lenola D et al (2016) Lateral inhibition in the somatosensory cortex during and between migraine without aura attacks: correlations with thalamocortical activity and clinical features. Cephalalgia 36:568–578
38. Höffken O, Stude P, Lenz M et al (2009) Visual paired-pulse stimulation reveals enhanced visual cortex excitability in migraineurs. Eur J Neurosci 30:714–720
39. Strigaro G, Cerino A, Falletta L et al (2015) Impaired visual inhibition in migraine with aura. Clin Neurophysiol 126:1988–1993
40. Bough KJ, Wetherington J, Hassel B et al (2006) Mitochondrial biogenesis in the anticonvulsant mechanism of the ketogenic diet. Ann Neurol 60:223–235
41. Maalouf M, Sullivan PG, Davis L et al (2007) Ketones inhibit mitochondrial production of reactive oxygen species production following glutamate excitotoxicity by increasing NADH oxidation. Neuroscience 145:256–264
42. Bough K (2008) Energy metabolism as part of the anticonvulsant mechanism of the ketogenic diet. Epilepsia 8:91–93
43. Kim DO, Vallejo J, Rho JM (2010) Ketones prevent synaptic dysfunction induced by mitochondrial respiratory complex inhibitors. J Neurochem 114:130–141
44. Barbiroli B, Montagna P, Cortelli P et al (1992) Abnormal brain and muscle energy metabolism shown by 31P magnetic resonance spectroscopy in patients affected by migraine with aura. Neurology 42:1209–1214
45. Sándor P, Dydak U, Schoenen J et al (2005) MR-spectroscopic imaging during visual stimulation in subgroups of migraine with aura. Cephalalgia 25:507–518
46. Di Lorenzo C, Pierelli F, Coppola G et al (2009) Mitochondrial DNA haplogroups influence the therapeutic response to riboflavin in migraineurs. Neurology 72:1588–1594
47. Sappey-Marinier D, Calabrese G, Fein G et al (1992) Effect of photic stimulation on human visual cortex lactate and phosphates using 1H and 31P magnetic resonance spectroscopy. J Cereb Blood Flow Metab 12:584–592
48. Jackson MJ, Schaefer JA, Johnson MA et al (1995) Presentation and clinical investigation of mitochondrial respiratory chain disease. A study of 51 patients. Brain 118:339–357
49. Ambrosini A, Coppola G, Iezzi E et al (2016) Reliability and repeatability of testing visual evoked potential habituation in migraine: A blinded case–control study. Cephalalgia. doi:10.1177/0333102416648656
50. Kossoff EH, Hartman AL (2012) Ketogenic diets: new advances for metabolism-based therapies. Curr Opin Neurol 25:173–178