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Review Article

Novelty in Inflammation and Immunomodulation in Migraine

Author(s): Cinzia Cavestro*, Marcella Ferrero, Silvia Mandrino, Marco Di Tavi and Eugenia Rota

Volume 25, Issue 27, 2019

Page: [2919 - 2936] Pages: 18

DOI: 10.2174/1381612825666190709204107

Price: $65

Abstract

Background: Migraine is a diffuse and disabling disease. Its pathophysiology is complex and involves both central and peripheral dysfunctions.

Objective: This review will discuss the pathogenesis of migraine from the origin of the neuro-inflammatory theory, to the modern pathophysiological model and the latest therapies.

Methods: PUBMED and EMBASE (up to May 2019) were searched for: migraine, inflammation, immunomodulation. An additional search was carried out from the bibliography of previous review articles.

Results: Migraine was thought to be mainly a vascular disorder, according to the so-called “vascular theory”. Based on animal models, a new hypothesis called “the neuro-inflammatory” was conceived at the end of the 20th century. The growing knowledge about the trigeminovascular system and its role in the inflammatory-pain pathway, allowed to identify other specific neurotransmitters, such as the Calcitonin Gene-Related Peptide and Pituitary Adenylate Cyclase-Activating Peptide. Evidence was provided that the inflammatory-pain system could become sensitised and, due to this sensitisation, the pain could also perpetuate, even in the absence of any triggers of the migraine attack. At last, brain immune cells modification during cortical spreading depression in migraine was demonstrated, along with the existence and function of the glymphatic system. The better comprehension of the immune system abnormalities allowed the development of new immunomodulating drugs: the monoclonal antibodies against the CGRP or the CGRP receptor. Moreover, new insights into the molecular mechanism of CGRP, and the function of C-fibres and Aδ-fibres, highlighted the mechanism of action of Botulinum Toxin type A in the treatment of chronic migraine.

Keywords: Inflammation, neuroinflammation, immunomodulation, migraine, CGRP, botulinum toxin, monoclonal antibodies anti-CGRP.

« Previous Next »
[1]
Lipton RB, Stewart WF, Diamond S, Diamond ML, Reed M. Prevalence and burden of migraine in the United States: Data from the American Migraine Study II. Headache 2001; 41(7): 646-57.
[http://dx.doi.org/10.1046/j.1526-4610.2001.041007646.x] [PMID: 11554952]
[2]
Headache Classification Committee of the International Headache Society; The international classification of headache disorders. 3rd edition.. Cephalalgia. 2018; 38: pp. 1-211.
[3]
Weiller C, May A, Limmroth V, et al. Brain stem activation in spontaneous human migraine attacks. Nat Med 1995; 1(7): 658-60.
[http://dx.doi.org/10.1038/nm0795-658] [PMID: 7585147]
[4]
Bahra A, Matharu MS, Buchel C, Frackowiak RS, Goadsby PJ. Brainstem activation specific to migraine headache. Lancet 2001; 357(9261): 1016-7.
[http://dx.doi.org/10.1016/S0140-6736(00)04250-1] [PMID: 11293599]
[5]
Goadsby PJ, Charbit AR, Andreou AP, Akerman S, Holland PR. Neurobiology of migraine. Neuroscience 2009; 161(2): 327-41.
[http://dx.doi.org/10.1016/j.neuroscience.2009.03.019] [PMID: 19303917]
[6]
Olesen J, Burstein R, Ashina M, Tfelt-Hansen P. Origin of pain in migraine: Evidence for peripheral sensitisation. Lancet Neurol 2009; 8(7): 679-90.
[http://dx.doi.org/10.1016/S1474-4422(09)70090-0] [PMID: 19539239]
[7]
Ho TW, Edvinsson L, Goadsby PJ. CGRP and its receptors provide new insights into migraine pathophysiology. Nat Rev Neurol 2010; 6(10): 573-82.
[http://dx.doi.org/10.1038/nrneurol.2010.127] [PMID: 20820195]
[8]
Strassman AM, Levy D. Response properties of dural nociceptors in relation to headache. J Neurophysiol 2006; 95(3): 1298-306.
[http://dx.doi.org/10.1152/jn.01293.2005] [PMID: 16492942]
[9]
Graham J, Wolff H. Mechanism of migraine headache and action of ergotamine tartrate. Arch Neurol 1938; 39: 737-63.
[http://dx.doi.org/10.1001/archneurpsyc.1938.02270040093005]
[10]
Welch KM. Stroke and migraine--the spectrum of cause and effect. Funct Neurol 2003; 18(3): 121-6.
[PMID: 14703893]
[11]
Moskowitz MA. The neurobiology of vascular head pain. Ann Neurol 1984; 16(2): 157-68.
[http://dx.doi.org/10.1002/ana.410160202] [PMID: 6206779]
[12]
Williamson DJ, Hargreaves RJ. Neurogenic inflammation in the context of migraine. Microsc Res Tech 2001; 53(3): 167-78.
[http://dx.doi.org/10.1002/jemt.1081] [PMID: 11301492]
[13]
Moskowitz MA, Reinhard JF Jr, Romero J, Melamed E, Pettibone DJ. Neurotransmitters and the fifth cranial nerve: Is there a relation to the headache phase of migraine? Lancet 1979; 2(8148): 883-5.
[http://dx.doi.org/10.1016/S0140-6736(79)92692-8] [PMID: 90971]
[14]
Moskowitz MA. Neurogenic inflammation in the pathophysiology and treatment of migraine. Neurology 1993; 43(6)(Suppl. 3): S16-20.
[PMID: 8389008]
[15]
Akerman S, Holland PR, Hoffmann J. Pearls and pitfalls in experimental in vivo models of migraine: Dural trigeminovascular nociception. Cephalalgia 2013; 33(8): 577-92.
[http://dx.doi.org/10.1177/0333102412472071] [PMID: 23671254]
[16]
Barnes PJ, Belvisi MG, Rogers DF. Modulation of neurogenic inflammation: Novel approaches to inflammatory disease. Trends Pharmacol Sci 1990; 11(5): 185-9.
[http://dx.doi.org/10.1016/0165-6147(90)90112-L] [PMID: 2248639]
[17]
Holzer P. Neurogenic vasodilatation and plasma leakage in the skin. Gen Pharmacol 1998; 30(1): 5-11.
[http://dx.doi.org/10.1016/S0306-3623(97)00078-5] [PMID: 9457475]
[18]
Lembeck F, Holzer P. Substance P as neurogenic mediator of antidromic vasodilation and neurogenic plasma extravasation. Naunyn Schmiedebergs Arch Pharmacol 1979; 310(2): 175-83.
[http://dx.doi.org/10.1007/BF00500282] [PMID: 93706]
[19]
Jansen I, Alafaci C, McCulloch J, Uddman R, Edvinsson L. Tachykinins (substance P, neurokinin A, neuropeptide K, and neurokinin B) in the cerebral circulation: Vasomotor responses in vitro and in situ. J Cereb Blood Flow Metab 1991; 11(4): 567-75.
[http://dx.doi.org/10.1038/jcbfm.1991.105] [PMID: 1711051]
[20]
Brain SD, Williams TJ, Tippins JR, Morris HR, MacIntyre I. Calcitonin gene-related peptide is a potent vasodilator. Nature 1985; 313(5997): 54-6.
[http://dx.doi.org/10.1038/313054a0] [PMID: 3917554]
[21]
Markowitz S, Saito K, Moskowitz MA. Neurogenically mediated leakage of plasma protein occurs from blood vessels in dura mater but not brain. J Neurosci 1987; 7(12): 4129-36.
[http://dx.doi.org/10.1523/JNEUROSCI.07-12-04129.1987] [PMID: 3694267]
[22]
Dimitriadou V, Buzzi MG, Moskowitz MA, Theoharides TC. Trigeminal sensory fiber stimulation induces morphological changes reflecting secretion in rat dura mater mast cells. Neuroscience 1991; 44(1): 97-112.
[http://dx.doi.org/10.1016/0306-4522(91)90253-K] [PMID: 1771000]
[23]
Matsubara T, Moskowitz MA, Huang Z. UK-14,304, R(-)-alpha-methyl-histamine and SMS 201-995 block plasma protein leakage within dura mater by prejunctional mechanisms. Eur J Pharmacol 1992; 224(2-3): 145-50.
[http://dx.doi.org/10.1016/0014-2999(92)90798-9] [PMID: 1281776]
[24]
Buzzi MG, Sakas DE, Moskowitz MA. Indomethacin and acetylsalicylic acid block neurogenic plasma protein extravasation in rat dura mater. Eur J Pharmacol 1989; 165(2-3): 251-8.
[http://dx.doi.org/10.1016/0014-2999(89)90719-X] [PMID: 2776831]
[25]
Moskowitz MA, Macfarlane R. Neurovascular and molecular mechanisms in migraine headaches. Cerebrovasc Brain Metab Rev 1993; 5(3): 159-77.
[PMID: 8217498]
[26]
Lee WS, Limmroth V, Ayata C, et al. Peripheral GABAA receptor-mediated effects of sodium valproate on dural plasma protein extravasation to substance P and trigeminal stimulation. Br J Pharmacol 1995; 116(1): 1661-7.
[http://dx.doi.org/10.1111/j.1476-5381.1995.tb16388.x] [PMID: 8564234]
[27]
Buzzi MG, Dimitriadou V, Theoharides TC, Moskowitz MA. 5-Hydroxytryptamine receptor agonists for the abortive treatment of vascular headaches block mast cell, endothelial and platelet activation within the rat dura mater after trigeminal stimulation. Brain Res 1992; 583(1-2): 137-49.
[http://dx.doi.org/10.1016/S0006-8993(10)80017-4] [PMID: 1324091]
[28]
Shepheard SL, Williamson DJ, Hill RG, Hargreaves RJ. The non-peptide neurokinin1 receptor antagonist, RP 67580, blocks neurogenic plasma extravasation in the dura mater of rats. Br J Pharmacol 1993; 108(1): 11-2.
[http://dx.doi.org/10.1111/j.1476-5381.1993.tb13432.x] [PMID: 7679023]
[29]
Jansen I, Uddman R, Ekman R, Olesen J, Ottosson A, Edvinsson L. Distribution and effects of neuropeptide Y, vasoactive intestinal peptide, substance P, and calcitonin gene-related peptide in human middle meningeal arteries: Comparison with cerebral and temporal arteries. Peptides 1992; 13(3): 527-36.
[http://dx.doi.org/10.1016/0196-9781(92)90084-G] [PMID: 1381830]
[30]
Ramachandran R. Neurogenic inflammation and its role in migraine. Semin Immunopathol 2018; 40(3): 301-14.
[http://dx.doi.org/10.1007/s00281-018-0676-y] [PMID: 29568973]
[31]
Levy D, Strassman AM. Mechanical response properties of A and C primary afferent neurons innervating the rat intracranial dura. J Neurophysiol 2002; 88(6): 3021-31.
[http://dx.doi.org/10.1152/jn.00029.2002] [PMID: 12466427]
[32]
Strassman AM, Raymond SA, Burstein R. Sensitization of meningeal sensory neurons and the origin of headaches. Nature 1996; 384(6609): 560-4.
[http://dx.doi.org/10.1038/384560a0] [PMID: 8955268]
[33]
Ray B, Wolff H. Experimental studies on headache: Pain-sensitive structures of the head and their significance in headache. Arch Surg 1940; 41: 813-56.
[http://dx.doi.org/10.1001/archsurg.1940.01210040002001]
[34]
Edvinsson L, Uddman R. Neurobiology in primary headaches. Brain Res Brain Res Rev 2005; 48(3): 438-56.
[http://dx.doi.org/10.1016/j.brainresrev.2004.09.007] [PMID: 15914251]
[35]
Procacci P, Maresca M. Referred pain from somatic and visceral structures: A reappraisal. Curr Rev Pain 1999; 3: 96-9.
[http://dx.doi.org/10.1007/s11916-999-0032-y]
[36]
Edvinsson L. Sensory nerves in man and their role in primary headaches. Cephalalgia 2001; 21(7): 761-4.
[http://dx.doi.org/10.1177/033310240102100705] [PMID: 11595008]
[37]
Burstein R, Yamamura H, Malick A, Strassman AM. Chemical stimulation of the intracranial dura induces enhanced responses to facial stimulation in brain stem trigeminal neurons. J Neurophysiol 1998; 79(2): 964-82.
[http://dx.doi.org/10.1152/jn.1998.79.2.964] [PMID: 9463456]
[38]
Schueler M, Neuhuber WL, De Col R, Messlinger K. Innervation of rat and human dura mater and pericranial tissues in the parieto-temporal region by meningeal afferents. Headache 2014; 54(6): 996-1009.
[http://dx.doi.org/10.1111/head.12371] [PMID: 24673461]
[39]
Edvinsson L, Uddman R. Adrenergic, cholinergic and peptidergic nerve fibres in dura mater--involvement in headache? Cephalalgia 1981; 1(4): 175-9.
[http://dx.doi.org/10.1046/j.1468-2982.1981.0104175.x] [PMID: 6181893]
[40]
Ma QP, Hill R, Sirinathsinghji D. Colocalization of CGRP with 5-HT1B/1D receptors and substance P in trigeminal ganglion neurons in rats. Eur J Neurosci 2001; 13(11): 2099-104.
[http://dx.doi.org/10.1046/j.0953-816x.2001.01586.x] [PMID: 11422450]
[41]
Tajti J, Szok D, Majláth Z, Tuka B, Csáti A, Vécsei L. Migraine and neuropeptides. Neuropeptides 2015; 52: 19-30.
[http://dx.doi.org/10.1016/j.npep.2015.03.006] [PMID: 26094101]
[42]
Eftekhari S, Warfvinge K, Blixt FW, Edvinsson L. Differentiation of nerve fibers storing CGRP and CGRP receptors in the peripheral trigeminovascular system. J Pain 2013; 14(11): 1289-303.
[http://dx.doi.org/10.1016/j.jpain.2013.03.010] [PMID: 23958278]
[43]
Eftekhari S, Salvatore CA, Calamari A, Kane SA, Tajti J, Edvinsson L. Differential distribution of calcitonin gene-related peptide and its receptor components in the human trigeminal ganglion. Neuroscience 2010; 169(2): 683-96.
[http://dx.doi.org/10.1016/j.neuroscience.2010.05.016] [PMID: 20472035]
[44]
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): 567-74.
[http://dx.doi.org/10.1016/0006-291X(89)91757-9] [PMID: 2803320]
[45]
Miyata A, Jiang L, Dahl RD, et al. Isolation of a neuropeptide corresponding to the N-terminal 27 residues of the pituitary adenylate cyclase activating polypeptide with 38 residues (PACAP38). Biochem Biophys Res Commun 1990; 170(2): 643-8.
[http://dx.doi.org/10.1016/0006-291X(90)92140-U] [PMID: 2383262]
[46]
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.
[http://dx.doi.org/10.1111/j.1476-5381.2012.01871.x] [PMID: 22289055]
[47]
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): 64.
[http://dx.doi.org/10.1186/s10194-018-0893-8] [PMID: 30088106]
[48]
Dickson L, Finlayson K. VPAC and PAC receptors: From ligands to function. Pharmacol Ther 2009; 121(3): 294-316.
[http://dx.doi.org/10.1016/j.pharmthera.2008.11.006] [PMID: 19109992]
[49]
Amin FM, Asghar MS, Guo S, et al. Headache and prolonged dilatation of the middle meningeal artery by PACAP38 in healthy volunteers. Cephalalgia 2012; 32(2): 140-9.
[http://dx.doi.org/10.1177/0333102411431333] [PMID: 22174350]
[50]
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(Pt 3): 779-94.
[http://dx.doi.org/10.1093/brain/awt369] [PMID: 24501094]
[51]
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): 180-7.
[http://dx.doi.org/10.1212/WNL.0000000000002261] [PMID: 26674334]
[52]
Baun M, Pedersen MH, Olesen J, Jansen-Olesen I. Dural mast cell degranulation is a putative mechanism for headache induced by PACAP-38. Cephalalgia 2012; 32(4): 337-45.
[http://dx.doi.org/10.1177/0333102412439354] [PMID: 22421901]
[53]
Bhatt DK, Gupta S, Olesen J, Jansen-Olesen I. PACAP-38 infusion causes sustained vasodilation of the middle meningeal artery in the rat: Possible involvement of mast cells. Cephalalgia 2014; 34(11): 877-86.
[http://dx.doi.org/10.1177/0333102414523846] [PMID: 24563332]
[54]
Hendriksen E, van Bergeijk D, Oosting RS, Redegeld FA. Mast cells in neuroinflammation and brain disorders. Neurosci Biobehav Rev 2017; 79: 119-33.
[http://dx.doi.org/10.1016/j.neubiorev.2017.05.001] [PMID: 28499503]
[55]
Galli SJ. New concepts about the mast cell. N Engl J Med 1993; 328(4): 257-65.
[http://dx.doi.org/10.1056/NEJM199301283280408] [PMID: 8418407]
[56]
Artico M, Cavallotti C. Catecholaminergic and acetylcholine esterase containing nerves of cranial and spinal dura mater in humans and rodents. Microsc Res Tech 2001; 53(3): 212-20.
[http://dx.doi.org/10.1002/jemt.1085] [PMID: 11301496]
[57]
Strassman AM, Weissner W, Williams M, Ali S, Levy D. Axon diameters and intradural trajectories of the dural innervation in the rat. J Comp Neurol 2004; 473(3): 364-76.
[http://dx.doi.org/10.1002/cne.20106] [PMID: 15116396]
[58]
Orr EL, Pace KR. The significance of mast cells as a source of histamine in the mouse brain. J Neurochem 1984; 42(3): 727-32.
[http://dx.doi.org/10.1111/j.1471-4159.1984.tb02743.x] [PMID: 6693900]
[59]
Zhang XC, Strassman AM, Burstein R, Levy D. Sensitization and activation of intracranial meningeal nociceptors by mast cell mediators. J Pharmacol Exp Ther 2007; 322(2): 806-12.
[http://dx.doi.org/10.1124/jpet.107.123745] [PMID: 17483291]
[60]
Zhang XC, Levy D. Modulation of meningeal nociceptors mechanosensitivity by peripheral proteinase-activated receptor-2: The role of mast cells. Cephalalgia 2008; 28(3): 276-84.
[http://dx.doi.org/10.1111/j.1468-2982.2007.01523.x] [PMID: 18254896]
[61]
Levy D, Burstein R, Kainz V, Jakubowski M, Strassman AM. Mast cell degranulation activates a pain pathway underlying migraine headache. Pain 2007; 130(1-2): 166-76.
[http://dx.doi.org/10.1016/j.pain.2007.03.012] [PMID: 17459586]
[62]
Reuter U, Bolay H, Jansen-Olesen I, et al. Delayed inflammation in rat meninges: Implications for migraine pathophysiology. Brain 2001; 124(Pt 12): 2490-502.
[http://dx.doi.org/10.1093/brain/124.12.2490] [PMID: 11701602]
[63]
Cuesta MC, Quintero L, Pons H, Suarez-Roca H. Substance P and calcitonin gene-related peptide increase IL-1 beta, IL-6 and TNF alpha secretion from human peripheral blood mononuclear cells. Neurochem Int 2002; 40(4): 301-6.
[http://dx.doi.org/10.1016/S0197-0186(01)00094-8] [PMID: 11792459]
[64]
Levite M. Neuropeptides, by direct interaction with T cells, induce cytokine secretion and break the commitment to a distinct T helper phenotype. Proc Natl Acad Sci USA 1998; 95(21): 12544-9.
[http://dx.doi.org/10.1073/pnas.95.21.12544] [PMID: 9770522]
[65]
Benveniste EN. Inflammatory cytokines within the central nervous system: Sources, function, and mechanism of action. Am J Physiol 1992; 263(1 Pt 1): C1-C16.
[PMID: 1636671]
[66]
Benveniste EN. Cytokine actions in the central nervous system. Cytokine Growth Factor Rev 1998; 9(3-4): 259-75.
[http://dx.doi.org/10.1016/S1359-6101(98)00015-X] [PMID: 9918124]
[67]
Kemper RH, Meijler WJ, Korf J, Ter Horst GJ. Migraine and function of the immune system: A meta-analysis of clinical literature published between 1966 and 1999. Cephalalgia 2001; 21(5): 549-57.
[http://dx.doi.org/10.1046/j.1468-2982.2001.00196.x] [PMID: 11472381]
[68]
Perini F, D’Andrea G, Galloni E, et al. Plasma cytokine levels in migraineurs and controls. Headache 2005; 45(7): 926-31.
[http://dx.doi.org/10.1111/j.1526-4610.2005.05135.x] [PMID: 15985111]
[69]
Sarchielli P, Alberti A, Baldi A, et al. Proinflammatory cytokines, adhesion molecules, and lymphocyte integrin expression in the internal jugular blood of migraine patients without aura assessed ictally. Headache 2006; 46(2): 200-7.
[http://dx.doi.org/10.1111/j.1526-4610.2006.00337.x] [PMID: 16492228]
[70]
Martelletti P, Stirparo G, Morrone S, Rinaldi C, Giacovazzo M. Inhibition of intercellular adhesion molecule-1 (ICAM-1), soluble ICAM-1 and interleukin-4 by nitric oxide expression in migraine patients. J Mol Med (Berl) 1997; 75(6): 448-53.
[http://dx.doi.org/10.1007/s001090050130] [PMID: 9231885]
[71]
Martelletti P, Morrone S. The role of adhesion molecules in migraine: A debate. Cephalalgia 2000; 20(2): 136.
[http://dx.doi.org/10.1046/j.1468-2982.2000.00027.x] [PMID: 10961772]
[72]
Empl M, Sostak P, Breckner M, et al. T-cell subsets and expression of integrins in peripheral blood of patients with migraine. Cephalalgia 1999; 19(8): 713-7.
[http://dx.doi.org/10.1046/j.1468-2982.1999.019008713.x] [PMID: 10570725]
[73]
Sarchielli P, Alberti A, Codini M, Floridi A, Gallai V. Nitric oxide metabolites, prostaglandins and trigeminal vasoactive peptides in internal jugular vein blood during spontaneous migraine attacks. Cephalalgia 2000; 20(10): 907-18.
[http://dx.doi.org/10.1046/j.1468-2982.2000.00146.x] [PMID: 11304026]
[74]
Levite M, Cahalon L, Hershkoviz R, Steinman L, Lider O. Neuropeptides, via specific receptors, regulate T cell adhesion to fibronectin. J Immunol 1998; 160(2): 993-1000.
[PMID: 9551939]
[75]
Gerring ZF, Powell JE, Montgomery GW, Nyholt DR. Genome-wide analysis of blood gene expression in migraine implicates immune-inflammatory pathways. Cephalalgia 2018; 38(2): 292-303.
[http://dx.doi.org/10.1177/0333102416686769] [PMID: 28058943]
[76]
Cavestro C, Ferrero M. Migraine in systemic autoimmune diseases. Endocr Metab Immune Disord Drug Targets 2018; 18(2): 124-34.
[http://dx.doi.org/10.2174/1871530317666171124124340] [PMID: 29173190]
[77]
Noseda R, Burstein R. Migraine pathophysiology: anatomy of the trigeminovascular pathway and associated neurological symptoms, CSD, sensitization and modulation of pain. Pain 2013; 154(Suppl. 1): S44-53.
[78]
Close LN, Eftekhari S, Wang M, Charles AC, Russo AF. Cortical spreading depression as a site of origin for migraine: Role of CGRP. Cephalalgia 2019; 39(3): 428-34.
[http://dx.doi.org/10.1177/0333102418774299] [PMID: 29695168]
[79]
Schain AJ, Melo-Carrillo A, Borsook D, Grutzendler J, Strassman AM, Burstein R. Activation of pial and dural macrophages and dendritic cells by cortical spreading depression. Ann Neurol 2018; 83(3): 508-21.
[http://dx.doi.org/10.1002/ana.25169] [PMID: 29394508]
[80]
Jessen NA, Munk AS, Lundgaard I, Nedergaard M. The glymphatic system: A beginner’s guide. Neurochem Res 2015; 40(12): 2583-99.
[http://dx.doi.org/10.1007/s11064-015-1581-6] [PMID: 25947369]
[81]
Schain AJ, Melo-Carrillo A, Strassman AM, Burstein R. Cortical spreading depression closes paravascular space and impairs glymphatic flow: Implications for migraine headache. J Neurosci 2017; 37(11): 2904-15.
[http://dx.doi.org/10.1523/JNEUROSCI.3390-16.2017] [PMID: 28193695]
[82]
Albrecht DS, Mainero C, Ichijo E, et al. Imaging of neuroinflammation in migraine with aura: A [11C]PBR28 PET/MRI study. Neurology 2019; 92(17): e2038-50.
[http://dx.doi.org/10.1212/WNL.0000000000007371] [PMID: 30918090]
[83]
Loggia ML, Chonde DB, Akeju O, et al. Evidence for brain glial activation in chronic pain patients. Brain 2015; 138(Pt 3): 604-15.
[http://dx.doi.org/10.1093/brain/awu377] [PMID: 25582579]
[84]
Mainero C, Boshyan J, Hadjikhani N. Altered functional magnetic resonance imaging resting-state connectivity in periaqueductal gray networks in migraine. Ann Neurol 2011; 70(5): 838-45.
[http://dx.doi.org/10.1002/ana.22537] [PMID: 22162064]
[85]
Pirazzini M, Rossetto O, Eleopra R, Montecucco C. Botulinum neurotoxins: Biology, pharmacology, and toxicology. Pharmacol Rev 2017; 69(2): 200-35.
[http://dx.doi.org/10.1124/pr.116.012658] [PMID: 28356439]
[86]
Webb RP. Engineering of botulinum neurotoxins for biomedical applications. Toxins (Basel) 2018; 10(6)E231
[http://dx.doi.org/10.3390/toxins10060231] [PMID: 29882791]
[87]
Pellizzari R, Rossetto O, Schiavo G, Montecucco C. Tetanus and botulinum neurotoxins: Mechanism of action and therapeutic uses. Philos Trans R Soc Lond B Biol Sci 1999; 354(1381): 259-68.
[http://dx.doi.org/10.1098/rstb.1999.0377] [PMID: 10212474]
[88]
Currà A, Berardelli A. Do the unintended actions of botulinum toxin at distant sites have clinical implications? Neurology 2009; 72(12): 1095-9.
[http://dx.doi.org/10.1212/01.wnl.0000345010.98495.fc] [PMID: 19307544]
[89]
Bozzi Y, Costantin L, Antonucci F, Caleo M. Action of botulinum neurotoxins in the central nervous system: Antiepileptic effects. Neurotox Res 2006; 9(2-3): 197-203.
[http://dx.doi.org/10.1007/BF03033939] [PMID: 16785118]
[90]
Aoki KR. Evidence for antinociceptive activity of botulinum toxin type A in pain management. Headache 2003; 43(Suppl. 1): S9-S15.
[http://dx.doi.org/10.1046/j.1526-4610.43.7s.3.x] [PMID: 12887389]
[91]
Blumenfeld A, Silberstein SD, Dodick DW, Aurora SK, Turkel CC, Binder WJ. Method of injection of onabotulinumtoxinA for chronic migraine: A safe, well-tolerated, and effective treatment paradigm based on the PREEMPT clinical program. Headache 2010; 50(9): 1406-18.
[http://dx.doi.org/10.1111/j.1526-4610.2010.01766.x] [PMID: 20958294]
[92]
Aurora SK, Winner P, Freeman MC, et al. OnabotulinumtoxinA for treatment of chronic migraine: Pooled analyses of the 56-week PREEMPT clinical program. Headache 2011; 51(9): 1358-73.
[http://dx.doi.org/10.1111/j.1526-4610.2011.01990.x] [PMID: 21883197]
[93]
Cernuda-Morollón E, Ramón C, Martínez-Camblor P, Serrano-Pertierra E, Larrosa D, Pascual J. OnabotulinumtoxinA decreases interictal CGRP plasma levels in patients with chronic migraine. Pain 2015; 156(5): 820-4.
[http://dx.doi.org/10.1097/j.pain.0000000000000119] [PMID: 25735000]
[94]
Domínguez C, Vieites-Prado A, Pérez-Mato M, et al. CGRP and PTX3 as predictors of efficacy of onabotulinumtoxin type A in chronic migraine: An observational study. Headache 2018; 58(1): 78-87.
[http://dx.doi.org/10.1111/head.13211] [PMID: 29131327]
[95]
Burstein R, Zhang X, Levy D, Aoki KR, Brin MF. Selective inhibition of meningeal nociceptors by botulinum neurotoxin type A: Therapeutic implications for migraine and other pains. Cephalalgia 2014; 34(11): 853-69.
[http://dx.doi.org/10.1177/0333102414527648] [PMID: 24694964]
[96]
Zhang X, Strassman AM, Novack V, Brin MF, Burstein R. Extracranial injections of botulinum neurotoxin type A inhibit intracranial meningeal nociceptors’ responses to stimulation of TRPV1 and TRPA1 channels: Are we getting closer to solving this puzzle? Cephalalgia 2016; 36(9): 875-86.
[http://dx.doi.org/10.1177/0333102416636843] [PMID: 26984967]
[97]
Nassini R, Materazzi S, Benemei S, Geppetti P. The TRPA1 channel in inflammatory and neuropathic pain and migraine. Rev Physiol Biochem Pharmacol 2014; 167: 1-43.
[http://dx.doi.org/10.1007/112_2014_18] [PMID: 24668446]
[98]
Benemei S, Dussor G. TRP channels and migraine: Recent developments and new therapeutic opportunities. Pharmaceuticals (Basel) 2019; 12(2)E54
[http://dx.doi.org/10.3390/ph12020054] [PMID: 30970581]
[99]
Matak I, Tékus V, Bölcskei K, Lacković Z, Helyes Z. Involvement of substance P in the antinociceptive effect of botulinum toxin type A: Evidence from knockout mice. Neuroscience 2017; 358: 137-45.
[http://dx.doi.org/10.1016/j.neuroscience.2017.06.040] [PMID: 28673722]
[100]
Edvinsson J, Warfvinge K, Edvinsson L. Modulation of inflammatory mediators in the trigeminal ganglion by botulinum neurotoxin type A: An organ culture study. J Headache Pain 2015; 16: 555.
[http://dx.doi.org/10.1186/s10194-015-0555-z] [PMID: 26245187]
[101]
Charles A. The pathophysiology of migraine: Implications for clinical management. Lancet Neurol 2018; 17(2): 174-82.
[http://dx.doi.org/10.1016/S1474-4422(17)30435-0] [PMID: 29229375]
[102]
Iyengar S, Johnson KW, Ossipov MH, Aurora SK. CGRP and the trigeminal system in migraine. Headache 2019; 59(5): 659-81.
[http://dx.doi.org/10.1111/head.13529] [PMID: 30982963]
[103]
Haanes KA, Edvinsson L. Pathophysiological mechanisms in migraine and the identification of new therapeutic targets. CNS Drugs 2019; 33(6): 525-37.
[http://dx.doi.org/10.1007/s40263-019-00630-6] [PMID: 30989485]
[104]
Steenbergh PH, Höppener JW, Zandberg J, Lips CJ, Jansz HS. A second human calcitonin/CGRP gene. FEBS Lett 1985; 183(2): 403-7.
[http://dx.doi.org/10.1016/0014-5793(85)80820-6] [PMID: 2985435]
[105]
Tso AR, Goadsby PJ. Anti-CGRP monoclonal antibodies: The next era of migraine prevention? Curr Treat Options Neurol 2017; 19(8): 27.
[http://dx.doi.org/10.1007/s11940-017-0463-4] [PMID: 28653227]
[106]
Grimsrud KW, Halker Singh RB. Emerging treatments in episodic migraine. Curr Pain Headache Rep 2018; 22(9): 61.
[http://dx.doi.org/10.1007/s11916-018-0716-2] [PMID: 30014208]
[107]
Zhu Y, Liu Y, Zhao J, Han Q, Liu L, Shen X. The efficacy and safety of calcitonin gene-related peptide monoclonal antibody for episodic migraine: A meta-analysis. Neurol Sci 2018; 39(12): 2097-106.
[http://dx.doi.org/10.1007/s10072-018-3547-3] [PMID: 30182284]
[108]
Dodick DW. CGRP ligand and receptor monoclonal antibodies for migraine prevention: Evidence review and clinical implications. Cephalalgia 2019; 39(3): 445-58.
[http://dx.doi.org/10.1177/0333102418821662] [PMID: 30661365]
[109]
Burch R, Rayhill M. New preventive treatments for migraine. BMJ 2018; 361: k2507.
[http://dx.doi.org/10.1136/bmj.k2507] [PMID: 29899031]
[110]
Krymchantowski AV, Krymchantowski AGF, Jevoux CDC. Migraine treatment: The doors for the future are open, but with caution and prudence. Arq Neuropsiquiatr 2019; 77(2): 115-21.
[http://dx.doi.org/10.1590/0004-282x20190004] [PMID: 30810596]
[111]
Kielbasa W, Helton DL. A new era for migraine: Pharmacokinetic and pharmacodynamic insights into monoclonal antibodies with a focus on galcanezumab, an anti-CGRP antibody. Cephalalgia 2019; 39(10): 1284-97.
[http://dx.doi.org/10.1177/0333102419840780] [PMID: 30917684]
[112]
Flessner MF, Lofthouse J. Zakaria el-R. In vivo diffusion of immunoglobulin G in muscle: effects of binding, solute exclusion, and lymphatic removal. Am J Physiol 1997; 273(6): H2783-93.
[PMID: 9435615]
[113]
Amgen and Novartis. Aimovig: Highlights of prescribing information. www.accessdata.fda.gov/drugsatfda_docs/label/2019/761077s0011b1.pdf(2019, accessed March 2019)
[114]
Stauffer VL, Dodick DW, Zhang Q, Carter JN, Ailani J, Conley RR. Evaluation of galcanezumab for the prevention of episodic migraine: The EVOLVE-1 randomized clinical trial. JAMA Neurol 2018; 75(9): 1080-8.
[http://dx.doi.org/10.1001/jamaneurol.2018.1212] [PMID: 29813147]
[115]
Cohen-Barak O, Weiss S, Rasamoelisolo M, et al. A phase 1 study to assess the pharmacokinetics, safety, and tolerability of fremanezumab doses (225 mg, 675 mg and 900 mg) in Japanese and Caucasian healthy subjects. Cephalalgia 2018; 38(13): 1960-71.
[http://dx.doi.org/10.1177/0333102418771376] [PMID: 29667896]
[116]
Davda JP, Hansen RJ. Properties of a general PK/PD model of antibody-ligand interactions for therapeutic antibodies that bind to soluble endogenous targets. MAbs 2010; 2(5): 576-88.
[http://dx.doi.org/10.4161/mabs.2.5.12833] [PMID: 20676036]
[117]
Melo-Carrillo A, Noseda R, Nir RR, et al. Selective inhibition of trigeminovascular neurons by fremanezumab: A humanized monoclonal anti-CGRP antibody. J Neurosci 2017; 37(30): 7149-63.
[http://dx.doi.org/10.1523/JNEUROSCI.0576-17.2017] [PMID: 28642283]
[118]
Dodick DW. Migraine. Lancet 2018; 391: 1315-30.
[http://dx.doi.org/10.1016/S0140-6736(18)30478-1] [PMID: 29523342]
[119]
Edvinsson L. The trigeminovascular pathway: Role of CGRP and CGRP receptors in migraine. Headache 2017; 57(Suppl. 2): 47-55.
[http://dx.doi.org/10.1111/head.13081] [PMID: 28485848]
[120]
Hong P, Wu X, Liu Y. Calcitonin gene-related peptide monoclonal antibody for preventive treatment of episodic migraine: A meta analysis. Clin Neurol Neurosurg 2017; 154: 74-8.
[http://dx.doi.org/10.1016/j.clineuro.2017.01.009] [PMID: 28129635]
[121]
Sun H, Dodick DW, Silberstein S, et al. Safety and efficacy of AMG 334 for prevention of episodic migraine: A randomised, double-blind, placebo-controlled, phase 2 trial. Lancet Neurol 2016; 15(4): 382-90.
[http://dx.doi.org/10.1016/S1474-4422(16)00019-3] [PMID: 26879279]
[122]
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): 425-34.
[http://dx.doi.org/10.1016/S1474-4422(17)30083-2] [PMID: 28460892]
[123]
Goadsby PJ, Reuter U, Hallström Y, et al. A controlled trial of erenumab for episodic migraine. N Engl J Med 2017; 377(22): 2123-32.
[http://dx.doi.org/10.1056/NEJMoa1705848] [PMID: 29171821]
[124]
Dodick DW, Ashina M, Brandes JL, et al. ARISE: A Phase 3 randomized trial of erenumab for episodic migraine. Cephalalgia 2018; 38(6): 1026-37.
[http://dx.doi.org/10.1177/0333102418759786] [PMID: 29471679]
[125]
Goadsby PJ, Paemeleire K, Broessner G, et al. Efficacy and safety of erenumab (AMG334) in episodic migraine patients with prior preventive treatment failure: A subgroup analysis of a randomized, double-blind, placebo-controlled study. Cephalalgia 2019; 39(7): 817-26.
[http://dx.doi.org/10.1177/0333102419835459] [PMID: 30982348]
[126]
Lipton RB, Tepper SJ, Reuter U, et al. Erenumab in chronic migraine: Patient-reported outcomes in a randomized double-blind study. Neurology 2019; 92(19): e2250-60.
[http://dx.doi.org/10.1212/WNL.0000000000007452] [PMID: 30996060]
[127]
Bigal ME, Walter S, Rapoport AM. Fremanezumab as a preventive treatment for episodic and chronic migraine. Expert Rev Neurother 2019; 19(8): 719-28.
[http://dx.doi.org/10.1080/14737175.2019.1614742] [PMID: 31043094]
[128]
Bigal ME, Dodick DW, Rapoport AM, et al. Safety, tolerability, and efficacy of TEV-48125 for preventive treatment of high-frequency episodic migraine: A multicentre, randomised, double-blind, placebo-controlled, phase 2b study. Lancet Neurol 2015; 14(11): 1081-90.
[http://dx.doi.org/10.1016/S1474-4422(15)00249-5] [PMID: 26432182]
[129]
Silberstein SD, Dodick DW, Bigal ME, et al. Fremanezumab for the preventive treatment of chronic migraine. N Engl J Med 2017; 377(22): 2113-22.
[http://dx.doi.org/10.1056/NEJMoa1709038] [PMID: 29171818]
[130]
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.
[http://dx.doi.org/10.1001/jama.2018.4853] [PMID: 29800211]
[131]
Dodick DW, Goadsby PJ, Spierings EL, Scherer JC, Sweeney SP, Grayzel DS. Safety and efficacy of LY2951742, a monoclonal antibody to calcitonin gene-related peptide, for the prevention of migraine: A phase 2, randomised, double-blind, placebo-controlled study. Lancet Neurol 2014; 13(9): 885-92.
[http://dx.doi.org/10.1016/S1474-4422(14)70128-0] [PMID: 25127173]
[132]
Stauffer VL, Dodick DW, Zhang Q, Carter JN, Ailani J, Conley RR. Evaluation of galcanezumab for the prevention of episodic migraine: The EVOLVE-1 randomized clinical trial. JAMA Neurol 2018; 75(9): 1080-8.
[http://dx.doi.org/10.1001/jamaneurol.2018.1212] [PMID: 29813147]
[133]
Skljarevski V, Matharu M, Millen BA, Ossipov MH, Kim BK, Yang JY. 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): 1442-54.
[http://dx.doi.org/10.1177/0333102418779543] [PMID: 29848108]
[134]
Detke HC, Goadsby PJ, Wang S, Friedman DI, Selzler KJ, Aurora SK. Galcanezumab in chronic migraine: The randomized, double-blind, placebo-controlled REGAIN study. Neurology 2018; 91(24): e2211-21.
[http://dx.doi.org/10.1212/WNL.0000000000006640] [PMID: 30446596]
[135]
Dodick DW, Goadsby PJ, Silberstein SD, et al. Safety and efficacy of ALD403, an antibody to calcitonin gene-related peptide, for the prevention of frequent episodic migraine: A randomised, double-blind, placebo-controlled, exploratory phase 2 trial. Lancet Neurol 2014; 13(11): 1100-7.
[http://dx.doi.org/10.1016/S1474-4422(14)70209-1] [PMID: 25297013]
[136]
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): 6.
[http://dx.doi.org/10.1186/s10194-018-0955-y] [PMID: 30651064]
[137]
Zeller J, Poulsen KT, Sutton JE, et al. CGRP function-blocking antibodies inhibit neurogenic vasodilatation without affecting heart rate or arterial blood pressure in the rat. Br J Pharmacol 2008; 155(7): 1093-103.
[http://dx.doi.org/10.1038/bjp.2008.334] [PMID: 18776916]
[138]
Bigal ME, Walter S, Bronson M, Alibhoy A, Escandon R. Cardiovascular and hemodynamic parameters in women following prolonged CGRP inhibition using LBR-101, a monoclonal antibody against CGRP. Cephalalgia 2014; 34(12): 968-76.
[http://dx.doi.org/10.1177/0333102414527646] [PMID: 24662322]
[139]
Tringali G, Navarra P. Anti-CGRP and anti-CGRP receptor monoclonal antibodies as antimigraine agents. Potential differences in safety profile postulated on a pathophysiological basis. Peptides 2019; 116: 16-21.
[http://dx.doi.org/10.1016/j.peptides.2019.04.012] [PMID: 31018157]

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