2,541
Views
1
CrossRef citations to date
0
Altmetric
Review

Emerging drugs for the prevention of migraine

, &
Pages 271-280 | Received 31 May 2021, Accepted 13 Jul 2021, Published online: 27 Jul 2021

References

  • Lipton R, Stewart W, Diamond S, et al. Prevalence and burden of migraine in the United States: data from the American Migraine Study II. Headache. 2001;41(7):646–657.
  • Vos T, Lim SS, Abbafati C, et al. Global burden of 369 diseases and injuries in 204 countries and territories, 1990-2019: a systematic analysis for the global burden of disease study 2019. Lancet. 2020;396(10258):1204–1222.
  • Migraine — level 4 cause [Internet]. Institute for health metrics and evaluation. 2021 [cited 2021 Mar 31]. Available from: http://www.healthdata.org/results/gbd_summaries/2019/migraine-level-4-cause
  • Linde M, Gustavsson A, Stovner L, et al. The cost of headache disorders in Europe: the Eurolight project. Eur J Neurol. 2011;19(5):703–711.
  • Bigal M, Lipton R. Clinical course in migraine: conceptualizing migraine transformation. Neurology. 2008;71(11):848–855.
  • Natoli J, Manack A, Dean B, et al. Global prevalence of chronic migraine: a systematic review. Cephalalgia. 2010;30(5):599–609.
  • Goadsby P, Holland P, Martins-Oliveira M, et al. Pathophysiology of migraine: a disorder of sensory processing. Physiol Rev. 2017;97(2):553–622.
  • Ferrari M, Roon K, Lipton R, et al. Oral triptans (serotonin 5-HT 1B/1D agonists) in acute migraine treatment: a meta-analysis of 53 trials. Lancet. 2001;358(9294):1668–1675.
  • Hepp Z, Bloudek L, Varon S. Systematic review of migraine prophylaxis adherence and persistence. J Managed Care Pharm. 2014;20(1):22–33.
  • Aurora S, Dodick D, Turkel C, et al. OnabotulinumtoxinA for treatment of chronic migraine: results from the double-blind, randomized, placebo-controlled phase of the PREEMPT 1 trial. Cephalalgia. 2010;30(7):793–803.
  • Diener H, Dodick D, Aurora S, et al. OnabotulinumtoxinA for treatment of chronic migraine: results from the double-blind, randomized, placebo-controlled phase of the PREEMPT 2 trial. Cephalalgia. 2010;30(7):804–814.
  • Ho T, Edvinsson L, Goadsby P. CGRP and its receptors provide new insights into migraine pathophysiology. Nat Rev Neurol. 2010;6(10):573–582.
  • Dodick DW, Silberstein SD, Bigal ME, et al. Effect of fremanezumab compared with placebo for prevention of episodic migraine: a randomized clinical trial. JAMA. 2018;319(19):1999–2008.
  • Silberstein SD, Dodick DW, Bigal ME, et al. Fremanezumab for the preventive treatment of chronic migraine. N Engl J Med. 2017;377(22):2113–2122.
  • Goadsby PJ, Reuter U, Hallström Y, et al. A controlled trial of erenumab for episodic migraine. N Engl J Med. 2017;377(22):2123–2132.
  • Dodick DW, Ashina M, Brandes JL, et al. ARISE: a phase 3 randomized trial of erenumab for episodic migraine. Cephalalgia. 2018;38(6):1026–1037.
  • Tepper S, Ashina M, Reuter U, et al. Safety and efficacy of erenumab for preventive treatment of chronic migraine: a randomised, double-blind, placebo-controlled phase 2 trial. Lancet Neurol. 2017;16(6):425–434.
  • Stauffer VL, Dodick DW, Zhang Q, et al. Evaluation of galcanezumab for the prevention of episodic migraine: the EVOLVE-1 randomized clinical trial. JAMA Neurol. 2018;75(9):1080–1088.
  • Detke HC, Goadsby PJ, Wang S, et al. Galcanezumab in chronic migraine: the randomized, double-blind, placebo-controlled REGAIN study. Neurology. 2018;91(24):e2211–e2221.
  • Skljarevski V, Matharu M, Millen BA, et al. Efficacy and safety of galcanezumab for the prevention of episodic migraine: results of the EVOLVE-2 phase 3 randomized controlled clinical trial. Cephalalgia. 2018;38(8):1442–1454.
  • Ashina M, Saper J, Cady R, et al. Eptinezumab in episodic migraine: a randomized, double-blind, placebo-controlled study (PROMISE-1). Cephalalgia. 2020;40(3):241–254.
  • Lipton R, Goadsby P, Smith J, et al. Efficacy and safety of eptinezumab in patients with chronic migraine. Neurology. 2020;94(13):e1365–e1377.
  • Deen M, Correnti E, Kamm K, et al. Blocking CGRP in migraine patients – a review of pros and cons. J Headache Pain. 2017 Sep 25;18(1):96.
  • Do T, Guo S, Ashina M. Therapeutic novelties in migraine: new drugs, new hope? J Headache Pain. 2019;20:1.
  • Ornello R, Casalena A, Frattale I, et al. Real-life data on the efficacy and safety of erenumab in the Abruzzo region, central Italy. J Headache Pain. 2020;21(1):1.
  • MaassenVanDenBrink A, Meijer J, Villalón C, et al. Wiping out CGRP: potential cardiovascular risks. Trends Pharmacol Sci. 2016;37(9):779–788.
  • Loder E, Burch R. Who should try new antibody treatments for migraine? JAMA Neurol. 2018;75(9):1039.
  • Cohen J, Ning X, Kessler Y, et al. Immunogenicity of biologic therapies for migraine: a review of current evidence. J Headache Pain. 2021;22(1):1.
  • Ashina M, Goadsby P, Reuter U, et al. Long‐term efficacy and safety of erenumab in migraine prevention: results from a 5‐year, open‐label treatment phase of a randomized clinical trial. Eur J Neurol. 2021;28(5):1716–1725.
  • Reuter U, Goadsby PJ, Lanteri-Minet M, et al. Efficacy and tolerability of erenumab in patients with episodic migraine in whom two-to-four previous preventive treatments were unsuccessful: a randomised, double-blind, placebo-controlled, phase 3b study. Lancet. 2018;392(10161):2280–2287.
  • Ferrari M, Diener H, Ning X, et al. Fremanezumab versus placebo for migraine prevention in patients with documented failure to up to four migraine preventive medication classes (FOCUS): a randomised, double-blind, placebo-controlled, phase 3b trial. Lancet. 2019;394(10203):1030–1040.
  • Mulleners W, Kim B, Láinez M, et al. Safety and efficacy of galcanezumab in patients for whom previous migraine preventive medication from two to four categories had failed (CONQUER): a multicentre, randomised, double-blind, placebo-controlled, phase 3b trial. Lancet Neurol. 2020;19(10):814–825.
  • Sacco S, Bendtsen L, Ashina M, et al. European headache federation guideline on the use of monoclonal antibodies acting on the calcitonin gene related peptide or its receptor for migraine prevention. J Headache Pain. 2019;20:1.
  • Croop R, Lipton R, Kudrow D, et al. Oral rimegepant for preventive treatment of migraine: a phase 2/3, randomised, double-blind, placebo-controlled trial. Lancet. 2021;397(10268):51–60.
  • NURTEC ODT (Rimegepant) prescribing information. [cited 2021 Jan 21]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2020/212728s000lbl.pdf
  • Goadsby P, Dodick D, Ailani J, et al. Safety, tolerability, and efficacy of orally administered atogepant for the prevention of episodic migraine in adults: a double-blind, randomised phase 2b/3 trial. Lancet Neurol. 2020;19(9):727–737.
  • AIlani J, Lipton RB, Goadsby PJ, et al. Atogepant significantly reduces mean monthly migraine days in the phase 3 trial (ADVANCE) for the prevention of migraine. Cephalalgia. 2020;40(1S):14–15.
  • Miyata A, Arimura A, Dahl RR, et al. Isolation of a novel 38 residue-hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells. Biochem Biophys Res Commun. 1989;164(1):567–574.
  • Vaudry D, Falluel-Morel A, Bourgault S, et al. Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol Rev. 2009;61(3):283–357.
  • Arimura A, Somogyvári-Vigh A, Miyata A, et al. Tissue distribution of PACAP as determined by RIA: highly abundant in the rat brain and testes. Endocrinology. 1991;129(5):2787–2789.
  • Harmar AJ, Fahrenkrug J, Gozes I, et al. Pharmacology and functions of receptors for vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide: IUPHAR review 1. Br J Pharmacol. 2012;166(1):4–17.
  • Edvinsson L, Tajti J, Szalárdy L, et al. PACAP and its role in primary headaches. J Headache Pain. 2018;19(1):21.
  • Palkovits M, Somogyvári-Vigh A, Arimura A. Concentrations of pituitary adenylate cyclase activating polypeptide (PACAP) in human brain nuclei. Brain Res. 1995;699(1):116–120.
  • Fahrenkrug J, Hannibal J. Localisation of the neuropeptide PACAP and its receptors in the rat parathyroid and thyroid glands. Gen Comp Endocrinol. 2011;171(1):105–113.
  • Köves K, Kántor O, Scammell J, et al. PACAP colocalizes with luteinizing and follicle-stimulating hormone immunoreactivities in the anterior lobe of the pituitary gland. Peptides. 1998;19(6):1069–1072.
  • Moody T, Ito T, Osefo N, et al. VIP and PACAP: recent insights into their functions/roles in physiology and disease from molecular and genetic studies. Curr Opin Endocrinol Diabetes Obes. 2011;18(1):61–67.
  • Barberi M, Muciaccia B, Morelli M, et al. Expression localisation and functional activity of pituitary adenylate cyclase-activating polypeptide, vasoactive intestinal polypeptide and their receptors in mouse ovary. Reproduction. 2007;134(2):281–292.
  • Dickson L, Finlayson K. VPAC and PAC receptors: from ligands to function. Pharmacol Ther. 2009;121(3):294–316.
  • Banks WA, Kastin AJ, Komaki G, et al. Passage of pituitary adenylate cyclase activating polypeptide1-27 and pituitary adenylate cyclase activating polypeptide1-38 across the blood-brain barrier. J Pharmacol Exp Ther. 1993;267(2):690–696.
  • Tajti J, Uddman R, Edvinsson L. Neuropeptide localization in the ‘migraine generator’ region of the human brainstem. Cephalalgia. 2001;21(2):96–101.
  • Knutsson M, Edvinsson L. Distribution of mRNA for VIP and PACAP receptors in human cerebral arteries and cranial ganglia. NeuroReport. 2002;13(4):507–509.
  • Robert C, Bourgeais L, Arreto CD, et al. Paraventricular hypothalamic regulation of trigeminovascular mechanisms involved in headaches. J Neurosci. 2013;33(20):8827–8840.
  • Eftekhari S, Salvatore C, Johansson S, et al. Localization of CGRP, CGRP receptor, PACAP and glutamate in trigeminal ganglion. Relation to the blood–brain barrier. Brain Res. 2015;1600:93–109.
  • Rubio-Beltrán E, Correnti E, Deen M, et al. PACAP38 and PAC1 receptor blockade: a new target for headache? J Headache Pain. 2018; 19(1). DOI: https://doi.org/10.1186/s10194-018-0893-8
  • Akerman S, Goadsby PJ. Neuronal PAC1 receptors mediate delayed activation and sensitization of trigeminocervical neurons: relevance to migraine. Sci Transl Med. 2015;7:1–11.
  • Birk S, Sitarz JT, Petersen KA, et al. The effect of intravenous PACAP38 on cerebral hemodynamics in healthy volunteers. Regul Pept. 2007;140(3):185–191.
  • Schytz HW, Birk S, Wienecke T, et al. PACAP38 induces migraine-like attacks in patients with migraine without aura. Brain. 2009;132(1):16–25.
  • Amin FM, Asghar MS, Guo S, et al. Headache and prolonged dilatation of the middle meningeal artery by PACAP38 in healthy volunteers. Cephalalgia. 2012 Jan;32(2):140–149.
  • Amin FM, Hougaard A, Schytz HW, et al. Investigation of the pathophysiological mechanisms of migraine attacks induced by pituitary adenylate cyclase-activating polypeptide-38. Brain. 2014;137(3):779–794.
  • Amin FM, Hougaard A, Magon S, et al. Change in brain network connectivity during PACAP38-induced migraine attacks A resting-state functional MRI study. Neurology. 2016;86(2):180–187.
  • Tuka B, Helyes Z, Markovics A, et al. Alterations in PACAP-38-like immunoreactivity in the plasma during ictal and interictal periods of migraine patients. Cephalalgia. 2013;33(13):1085–1095.
  • Zagami A, Edvinsson L, Goadsby P. Pituitary adenylate cyclase activating polypeptide and migraine. Ann Clin Transl Neurol. 2014;1(12):1036–1040.
  • Ashina M, Dolezil D, Bonner JH. A phase 2, randomized, double-blind, placebo-controlled trial of AMG 301, a pituitary adenylate cyclase-activating polypeptide PAC1 receptor monoclonal antibody for migraine prevention. Cephalalgia. 2021;41(1):33–44.
  • Sakurai T, Amemiya A, Ishii M, et al. Orexins and orexin receptors: a family of hypothalamic neuropeptides and g protein-coupled receptors that regulate feeding behavior. Cell. 1998;92(4):573–585.
  • Holland PR, Holland PR. Biology of neuropeptides: orexinergic involvement in primary headache disorders. Headache. 2017;57(Suppl 2):76–88.
  • Bertels Z, Pradhan A. Emerging treatment targets for migraine and other headaches. Headache. 2019;59(S2):50–65.
  • Ferguson AV, Samson WK. The orexin/hypocretin system: a critical regulator of neuroendocrine and autonomic function. Front Neuroendocrinol. 2003;24(3):141–150.
  • Sarchielli P, Rainero I, Coppola F, et al. Involvement of corticotrophin-releasing factor and orexin-a in chronic migraine and medication-overuse headache: findings from cerebrospinal fluid. Cephalalgia. 2008;28(7):714–722.
  • Dahmen N, Kasten M, Wieczorek S, et al. Increased frequency of migraine in narcoleptic patients: a confirmatory study. Cephalalgia. 2003;23(1):14–19.
  • Rasmussen B, Jensen R, Schroll M, et al. Epidemiology of headache in a general population—A prevalence study. J Clin Epidemiol. 1991;44(11):1147–1157.
  • Breslau N, Davis GC, Andreski P. Migraine, psychiatric disorders, and suicide attempts: an epidemiologic study of young adults. Psychiatry Res. 1991;37:11–23.
  • Stewart WF, Wood C, Reed ML, et al. Cumulative lifetime migraine incidence in women and men. Cephalalgia. 2008;28:1170–1178.
  • Bartsch T, Levy MJ, Knight YE, et al. Differential modulation of nociceptive dural input to [hypocretin] orexin A and B receptor activation in the posterior hypothalamic area. Pain. 2004;109(3):367–378.
  • Holland PR, Akerman S, Goadsby PJ, Holland PR, Akerman S, Goadsby PJ. Orexin 1 receptor activation attenuates neurogenic dural vasodilation in an animal model of trigeminovascular nociception. J Pharmacol Exp Ther. 2005;315(3):1380–1385.
  • Holland PR, Akerman S, Goadsby PJ, Holland PR, Akerman S, Goadsby PJ. Modulation of nociceptive dural input to the trigeminal nucleus caudalis via activation of the orexin 1 receptor in the rat. Eur J Neurosci. 2006;24(10):2825–2833.
  • Hoffmann J, Supronsinchai W, Akerman S, et al. Evidence for orexinergic mechanisms in migraine. Neurobiol Dis. 2015;74:137–143.
  • Chabi A, Zhang Y, Jackson S, et al. Randomized controlled trial of the orexin receptor antagonist filorexant for migraine prophylaxis. Cephalalgia. 2015;35(5):379–388.
  • Goadsby PJ. Putting migraine to sleep: rexants as a preventive strategy. Cephalalgia. 2015;35(5):377–378.
  • Kew J, Kemp J. Ionotropic and metabotropic glutamate receptor structure and pharmacology. Psychopharmacology (Berl). 2005;179(1):4–29.
  • Bowes M, Panesar M, Gentry C, et al. Anti-hyperalgesic effects of the novel metabotropic glutamate receptor 5 antagonist, 2-methyl-6-(phenylethynyl)-pyridine, in rat models of inflammatory pain. Br J Pharmacol. 1999;126:250P.
  • Walker K, Reeve A, Bowes M, et al. mGlu5 receptors and nociceptive function II. mGlu5 receptors functionally expressed on peripheral sensory neurones mediate inflammatory hyperalgesia. Neuropharmacology. 2001;40:10–19.
  • Walker K, Bowes M, Panesar M, et al. Metabotropic glutamate receptor subtype 5 (mGlu5) and nociceptive function I. Selective blockade of mGlu5 receptors in models of acute, persistent and chronic pain. Neuropharmacology. 2001;40(1);1-9.
  • Niswender C, Conn P. Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu Rev Pharmacol Toxicol. 2010;50(1):295–322.
  • Ferrari MD, Odink J, Bos KD, et al. Neuroexcitatory plasma amino acids are elevated in migraine. Neurology. 1990;40:1582–1586.
  • Campos F, Sobrino T, Perez-Mato M, et al. Glutamate oxaloacetate transaminase: a new key in the dysregulation of glutamate in migraine patients. Cephalalgia. 2013;33:1148–1154.
  • Martinez F, Castillo J, Rodriguez JR, et al. Neuroexcitatory amino acid levels in plasma and cerebrospinal fluid during migraine attacks. Cephalalgia. 1993;13:89–93.
  • Peres MF, Zukerman E, Senne Soares CA, et al. Cerebrospinal fluid glutamate levels in chronic migraine. Cephalalgia. 2004;24:735–739.
  • Rajda C, Tajti J, Komoróczy R, et al. Amino acids in the saliva of patients with migraine. Headache. 1999;39:644–649.
  • Nam JH, Lee HS, Kim J, et al. Salivary glutamate is elevated in individuals with chronic migraine. Cephalalgia. 2018;38(8):1485–1492.
  • Baad-Hansen L, Cairns B, Ernberg M, et al. Effect of systemic monosodium glutamate (MSG) on headache and pericranial muscle sensitivity. Cephalalgia. 2010;30:68–76.
  • Yang WH, Drouin MA, Herbert M, et al. The monosodium glutamate symptom complex: assessment in a double-blind, placebo-controlled, randomized study. J Allergy Clin Immunol. 1997;99:757–762.
  • Bhave G, Karim F, Carlton SM, et al. Peripheral group I metabotropic glutamate receptors modulate nociception in mice. Nat Neurosci. 2001;4:417–423.
  • Li B, Lu L, Tan X, et al. Peripheral metabotropic glutamate receptor subtype 5 contributes to inflammation-induced hypersensitivity of the rat temporomandibular joint. J Mol Neurosci. 2013;51:710–718.
  • Waung MW, Akerman S, Wakefield M, et al. Metabotropic glutamate receptor 5: a target for migraine therapy. Ann Clin Transl Neurol. 2016;3:560–571.
  • Hoffmann J, Charles A. Glutamate and its receptors as therapeutic targets for migraine. Neurotherapeutics. 2018;15:361–370.
  • Kawasaki Y, Kohno T, Zhuang Z-Y, et al. Ionotropic and metabotropic receptors, protein kinase A, protein kinase C, and Src contribute to C-fiber-induced ERK activation and cAMP response element-binding protein phosphorylation in dorsal horn neurons, leading to central sensitization. J Neurosci. 2004;24:8310–8321.
  • Niu Y, Zeng X, Zhao L, et al. Metabotropic glutamate receptor 5 regulates synaptic plasticity in a chronic migraine rat model through the PKC/NR2B signal. J Headache Pain. 2020;21:1.
  • Rascol O, Fox S, Gasparini F, et al. Use of metabotropic glutamate 5‐receptor antagonists for treatment of levodopa‐induced dyskinesias. Parkinsonism Relat Disord. 2014;20:947–956.
  • Bryan NS, Bian K, Murad F. Discovery of the nitric oxide signaling pathway and targets for drug development. Front Biosci (Landmark Ed). 2009;14:1‐18.
  • Moncada S, Higgs EA. The discovery of nitric oxide and its role in vascular biology. Br J Pharmacol. 2006;147(Suppl. 1):S193‐ S201.
  • Pradhan AA, Bertels Z, Akerman S. Targeted Nitric oxide synthase inhibitors for migraine. Neurotherapeutics. 2018;15(2):391–401.
  • Sicuteri F, Del Bene E, Poggioni M, et al. Unmasking latent dysnociception in healthy subjects. Headache. 1987;27(4):180–185.
  • Akerman S, Karsan N, Bose P, et al. Nitroglycerine triggers triptan-responsive cranial allodynia and trigeminal neuronal hypersensitivity. Brain. 2019;142(1):103–119.
  • Ramachandran R, Ploug K, Hay-Schmidt A, et al. Nitric oxide synthase (NOS) in the trigeminal vascular system and other brain structures related to pain in rats. Neurosci Lett. 2010;484(3):192–196.
  • Dieterle A, Fischer M, Link A, et al. Increase in CGRP- and nNOS-immunoreactive neurons in the rat trigeminal ganglion after infusion of an NO donor. Cephalalgia. 2010;31(1):31–42.
  • Pardutz A, Krizbai I, Multon S, et al. Systemic nitroglycerin increases nNOS levels in rat trigeminal nucleus caudalis. NeuroReport. 2000;11(14):3071–3075.
  • Moncada S, Palmer RM, Higgs EA. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev. 1991;43:109‐142.
  • Palmer JE, Guillard FL, Laurijssens BE, et al. randomised, single-blind, placebo-controlled, adaptive clinical trial of GW274150, a selective iNOS inhibitor, in the treatment of acute migraine. Cephalalgia. 2009;29:124.
  • Høivik H, Laurijssens B, Harnisch L, et al. Lack of efficacy of the selective iNOS inhibitor GW274150 in prophylaxis of migraine headache. Cephalalgia. 2010;30(12):1458–1467.
  • Akerman S, Williamson D, Kaube H, et al. Nitric oxide synthase inhibitors can antagonize neurogenic and calcitonin gene-related peptide induced dilation of dural meningeal vessels. Br J Pharmacol. 2002;137(1):62–68.
  • Bhatt D, Gupta S, Jansen-Olesen I, et al. NXN-188, a selective nNOS inhibitor and a 5-HT1B/1D receptor agonist, inhibits CGRP release in preclinical migraine models. Cephalalgia. 2012;33(2):87–100.
  • De Felice M, Ossipov M, Wang R, et al. Triptan-induced enhancement of neuronal nitric oxide synthase in trigeminal ganglion dural afferents underlies increased responsiveness to potential migraine triggers. Brain. 2010;133(8):2475–2488.
  • Medve RA, Lategan TW. A phase 2 multicenter, randomized, double-blind, parallel-group, placebo-controlled study of NXN-188 dihydrochloride in acute migraine without aura [abstract 190]. Presented at the 2nd European headache and migraine trust international congress 2010. Nice, France, 28–31 October 2010. J Headache Pain. 2010;11:38.
  • Hougaard A, Hauge AW, Guo S, et al. The nitric oxide synthase inhibitor and serotonin-receptor agonist NXN-188 during the aura phase of migraine with aura: a randomized, double-blind, placebo-controlled cross-over study. Scand J Pain. 2013;4(1):48–52.
  • Hansen JM, Hauge AW, Olesen J, et al. Calcitonin gene-related peptide triggers migraine-like attacks in patients with migraine with aura. Cephalalgia. 2010;30:1179–1186.
  • Christopoulos A, Christopoulos G, Morfis M, et al. Novel receptor partners and function of receptor activity-modifying proteins. J Biol Chem. 2003;278(5):3293–3297.
  • Guo S, Vollesen AL, Hansen YB, et al. Part II: biochemical changes after pituitary adenylate cyclase‐activating polypeptide‐38 infusion in migraine patients. Cephalalgia. 2017;37:136‐147.