Renin-Angiotensin-Aldosterone System and Migraine: A Systematic Review of Human Studies

Author(s): Karina Lúcia Moreira Sassi, Laís Bhering Martins, Aline Silva de Miranda, Antonio Lucio Teixeira*

Journal Name: Protein & Peptide Letters

Volume 27 , Issue 6 , 2020


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Graphical Abstract:


Abstract:

Migraine is a common neurologic condition marked by recurrent episodes of headache. Its pathophysiology is highly complex involving neuronal, inflammatory and vascular mechanisms. The Renin-Angiotensin System (RAS) can modulate all these mechanism, being a potential pharmacological target for migraine treatment. We carried out a systematic review of the studies evaluating the involvement of RAS in patients with migraine. There is evidence from genetic studies exploring the relation between migraine and RAS-related genes and from clinical trials evaluating the efficacy of Angiotensin II Type 1 (AT1) receptor antagonists and angiotensin converting enzyme inhibitors in migraine prophylaxis. RAS seems to play a role in the pathophysiology of migraine, but more direct evidence is still missing.

Keywords: Renin, angiotensin, aldosterone, migraine, headache, genetics.

[1]
Charles, A. Migraine. N. Engl. J. Med., 2017, 377(6), 553-561.
[http://dx.doi.org/10.1056/NEJMcp1605502] [PMID: 28792865]
[2]
Detsky, M.E.; McDonald, D.R.; Baerlocher, M.O.; Tomlinson, G.A.; McCrory, D.C.; Booth, C.M. Does this patient with headache have a migraine or need neuroimaging? JAMA, 2006, 296(10), 1274-1283.
[http://dx.doi.org/10.1001/jama.296.10.1274] [PMID: 16968852]
[3]
Goadsby, P.J.; Lipton, R.B.; Ferrari, M.D. Migraine--current understanding and treatment. N. Engl. J. Med., 2002, 346(4), 257-270.
[http://dx.doi.org/10.1056/NEJMra010917] [PMID: 11807151]
[4]
Hildreth, C.J.; Lynm, C.; Glass, R.M. JAMA patient page. Migraine headache. JAMA, 2009, 301(24), 2608.
[http://dx.doi.org/10.1001/jama.301.24.2608] [PMID: 19549980]
[5]
Teixeira, A.L.; Costa, E.A.; da Silva, A.A., Jr; dos Santos, I.A.; Gómez, R.S.; Kummer, A.; Lauterbach, E.C. Psychiatric comorbidities of chronic migraine in community and tertiary care clinic samples. J. Headache Pain, 2012, 13(7), 551-555.
[http://dx.doi.org/10.1007/s10194-012-0480-3] [PMID: 22940870]
[6]
Hershey, A.D. CGRP - The next frontier for migraine. N. Engl. J. Med., 2017, 377(22), 2190-2191.
[http://dx.doi.org/10.1056/NEJMe1712559] [PMID: 29171812]
[7]
Al-Quliti, K.W.; Assaedi, E.S. New advances in prevention of migraine. Review of current practice and recent advances. Neurosciences (Riyadh), 2016, 21(3), 207-214.
[http://dx.doi.org/10.17712/nsj.2016.3.20150506] [PMID: 27356650]
[8]
Burch, R.; Rizzoli, P.; Loder, E. The prevalence and impact of migraine and severe headache in the United States: Figures and trends from government health studies. Headache, 2018, 58(4), 496-505.
[http://dx.doi.org/10.1111/head.13281] [PMID: 29527677]
[9]
Jhingran, P.; Osterhaus, J.T.; Miller, D.W.; Lee, J.T.; Kirchdoerfer, L. Development and validation of the migraine-specific quality of life questionnaire. Headache, 1998, 38(4), 295-302.
[http://dx.doi.org/10.1046/j.1526-4610.1998.3804295.x] [PMID: 9595870]
[10]
Láinez, M.J.; García-Casado, A.; Gascón, F. Optimal management of severe nausea and vomiting in migraine: improving patient outcomes. Patient Relat. Outcome Meas., 2013, 4, 61-73.
[http://dx.doi.org/10.2147/PROM.S31392] [PMID: 24143125]
[11]
Min, Y.W.; Lee, J.H.; Min, B.H.; Lee, J.H.; Kim, J.J.; Chung, C.S.; Rhee, P.L. Clinical predictors for migraine in patients presenting with nausea and/or vomiting. J. Neurogastroenterol. Motil., 2013, 19(4), 516-520.
[http://dx.doi.org/10.5056/jnm.2013.19.4.516] [PMID: 24199013]
[12]
Giffin, N.J.; Lipton, R.B.; Silberstein, S.D.; Olesen, J.; Goadsby, P.J. The migraine postdrome: An electronic diary study. Neurology, 2016, 87(3), 309-313.
[http://dx.doi.org/10.1212/WNL.0000000000002789] [PMID: 27335112]
[13]
DeLange, J.M.; Cutrer, F.M. Our evolving understanding of migraine with aura. Curr. Pain Headache Rep., 2014, 18(10), 453.
[http://dx.doi.org/10.1007/s11916-014-0453-0] [PMID: 25230799]
[14]
Park, J-W.; Chu, M.K.; Kim, J-M.; Park, S-G.; Cho, S-J. Analysis of trigger factors in episodic migraineurs using a smartphone headache diary applications. PLoS One, 2016, 11(2)e0149577
[http://dx.doi.org/10.1371/journal.pone.0149577] [PMID: 26901341]
[15]
Martin, P.R. Behavioral management of migraine headache triggers: learning to cope with triggers. Curr. Pain Headache Rep., 2010, 14(3), 221-227.
[http://dx.doi.org/10.1007/s11916-010-0112-z] [PMID: 20425190]
[16]
Gürsoy, A.E.; Ertaş, M. Prophylactic treatment of migraine. Noro Psikiyatri Arsivi, 2013, 50(Suppl. 1), S30-S35.
[17]
Demaagd, G. The pharmacological management of migraine, part 1: Overview and abortive therapy. P&T, 2008, 33(7), 404-416.
[PMID: 19750119]
[18]
D’Amico, D.; Tepper, S.J. Prophylaxis of migraine: general principles and patient acceptance. Neuropsychiatr. Dis. Treat., 2008, 4(6), 1155-1167.
[http://dx.doi.org/10.2147/NDT.S3497] [PMID: 19337456]
[19]
Martins, L.B. Double-blind placebo-controlled randomized clinical trial of ginger (Zingiber officinale Rosc.) in the prophylactic treatment of migraine. Cephalalgia, 2020, 40(1), 88-95.
[http://dx.doi.org/10.1177/0333102419869319]
[20]
Akkermans, R.; Wolff, H.G. Lancet Neurol., 2015, 14(10), 982-983.
[http://dx.doi.org/10.1016/S1474-4422(15)00184-2] [PMID: 26636144]
[21]
Mason, B.N.; Russo, A.F. Vascular contributions to migraine: Time to revisit? Front. Cell. Neurosci., 2018, 12, 233.
[http://dx.doi.org/10.3389/fncel.2018.00233] [PMID: 30127722]
[22]
Dalkara, T.; Nozari, A.; Moskowitz, M.A. Migraine aura pathophysiology: the role of blood vessels and microembolisation. Lancet Neurol., 2010, 9(3), 309-317.
[http://dx.doi.org/10.1016/S1474-4422(09)70358-8] [PMID: 20170844]
[23]
Noseda, R.; Burstein, R. Migraine pathophysiology: anatomy of the trigeminovascular pathway and associated neurological symptoms, CSD, sensitization and modulation of pain. Pain, 2013, 154(1), S44-S53.
[http://dx.doi.org/10.1016/j.pain.2013.07.021]
[24]
Tfelt-Hansen, P.C.; Koehler, P.J. History of the use of ergotamine and dihydroergotamine in migraine from 1906 and onward. Cephalalgia, 2008, 28(8), 877-886.
[http://dx.doi.org/10.1111/j.1468-2982.2008.01578.x] [PMID: 18460007]
[25]
Moher, D.; Liberati, A.; Tetzlaff, J.; Altman, D.G. PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med., 2009, 6(7) e1000097
[http://dx.doi.org/10.1371/journal.pmed.1000097] [PMID: 19621072]
[26]
Montgomery, L. Are angiotensin-Converting Enzyme (ACE) inhibitors effective in preventing migraine in nonhypertensive patients? J. Fam. Pract., 2001, 50(4), 299.
[PMID: 11300977]
[27]
Schrader, H.; Stovner, L.J.; Helde, G.; Sand, T.; Bovim, G. Prophylactic treatment of migraine with angiotensin converting enzyme inhibitor (lisinopril): randomised, placebo controlled, crossover study. BMJ, 2001, 322(7277), 19-22.
[http://dx.doi.org/10.1136/bmj.322.7277.19] [PMID: 11141144]
[28]
Tronvik, E.; Stovner, L.J.; Helde, G.; Sand, T.; Bovim, G. Prophylactic treatment of migraine with an angiotensin II receptor blocker: a randomized controlled trial. JAMA, 2003, 289(1), 65-69.
[http://dx.doi.org/10.1001/jama.289.1.65] [PMID: 12503978]
[29]
Charles, J.A.; Jotkowitz, S.; Byrd, L.H. Prevention of migraine with olmesartan in patients with hypertension/prehypertension. Headache, 2006, 46(3), 503-507.
[http://dx.doi.org/10.1111/j.1526-4610.2006.00382.x] [PMID: 16618270]
[30]
Diener, H.C.; Gendolla, A.; Feuersenger, A.; Evers, S.; Straube, A.; Schumacher, H.; Davidai, G. Telmisartan in migraine prophylaxis: a randomized, placebo-controlled trial. Cephalalgia, 2009, 29(9), 921-927.
[http://dx.doi.org/10.1111/j.1468-2982.2008.01825.x] [PMID: 19250283]
[31]
Rahimtoola, H.; Buurma, H.; Tijssen, C.C.; Leufkens, H.G.; Egberts, A.C. Reduction in the therapeutic intensity of abortive migraine drug use during ACE inhibition therapy--a pilot study. Pharmacoepidemiol. Drug Saf., 2004, 13(1), 41-47.
[http://dx.doi.org/10.1002/pds.893] [PMID: 14971122]
[32]
Ikeda, K.; Hanashiro, S.; Ishikawa, Y.; Sawada, M.; Kyuzen, M.; Morioka, H.; Ebina, J.; Nagasawa, J.; Yanagihashi, M.; Miura, K.; Hirayama, T.; Takazawa, T.; Kano, O.; Kawabe, K.; Iwasaki, Y. Treatment with telmisartan, a long-acting angiotensin II receptor blocker, prevents migraine attacks in Japanese non-responders to lomerizine. Neurol. Sci., 2017, 38(5), 827-831.
[http://dx.doi.org/10.1007/s10072-017-2854-4] [PMID: 28224326]
[33]
Schuh-Hofer, S.; Flach, U.; Meisel, A.; Israel, H.; Reuter, U.; Arnold, G. Efficacy of lisinopril in migraine prophylaxis--an open label study. Eur. J. Neurol., 2007, 14(6), 701-703.
[http://dx.doi.org/10.1111/j.1468-1331.2007.01764.x] [PMID: 17539955]
[34]
Haaland, K. Angiotensin II receptor antagonists against migraine in pregnancy: fatal outcome. J. Headache Pain, 2010, 11(2), 167-169.
[http://dx.doi.org/10.1007/s10194-009-0182-7] [PMID: 20063032]
[35]
Disco, C.; Maggioni, F.; Zanchin, G. Angiotensin II receptor blockers: a new possible treatment for chronic migraine? Neurol. Sci., 2015, 36(8), 1483-1485.
[http://dx.doi.org/10.1007/s10072-015-2217-y] [PMID: 25917398]
[36]
Kowa, H.; Fusayasu, E.; Ijiri, T.; Ishizaki, K.; Yasui, K.; Nakaso, K.; Kusumi, M.; Takeshima, T.; Nakashima, K. Association of the insertion/deletion polymorphism of the angiotensin I-converting enzyme gene in patients of migraine with aura. Neurosci. Lett., 2005, 374(2), 129-131.
[http://dx.doi.org/10.1016/j.neulet.2004.10.041] [PMID: 15644278]
[37]
Lea, R.A.; Ovcaric, M.; Sundholm, J.; Solyom, L.; Macmillan, J.; Griffiths, L.R. Genetic variants of angiotensin converting enzyme and methylenetetrahydrofolate reductase may act in combination to increase migraine susceptibility. Brain Res. Mol. Brain Res., 2005, 136(1-2), 112-117.
[http://dx.doi.org/10.1016/j.molbrainres.2005.01.006] [PMID: 15893594]
[38]
Lin, J-J.; Wang, P-J.; Chen, C-H.; Yueh, K-C.; Lin, S-Z.; Harn, H-J. Homozygous deletion genotype of angiotensin converting enzyme confers protection against migraine in man. Acta Neurol. Taiwan., 2005, 14(3), 120-125.,
[PMID: 16252613]
[39]
Kara, I.; Ozkok, E.; Aydin, M.; Orhan, N.; Cetinkaya, Y.; Gencer, M.; Kilic, G.; Tireli, H. Combined effects of ACE and MMP-3 polymorphisms on migraine development. Cephalalgia, 2007, 27(3), 235-243.
[http://dx.doi.org/10.1111/j.1468-2982.2006.01269.x] [PMID: 17381556]
[40]
Schürks, M.; Zee, R.Y.L.; Buring, J.E.; Kurth, T. Polymorphisms in the renin-angiotensin system and migraine in women. Headache, 2009, 49(2), 292-299.
[http://dx.doi.org/10.1111/j.1526-4610.2008.01287.x] [PMID: 19178574]
[41]
Tietjen, G.E.; Herial, N.A.; Utley, C.; White, L.; Yerga-Woolwine, S.; Joe, B. Association of von Willebrand factor activity with ACE I/D and MTHFR C677T polymorphisms in migraine. Cephalalgia, 2009, 29(9), 960-968.
[http://dx.doi.org/10.1111/j.1468-2982.2008.01824.x] [PMID: 19298544]
[42]
Sipahi, T.; Güldiken, B.; Kabayel, L.; Palabiyik, O.; Özkan, H.; Kiliç, T.O.; Süt, N.; Turgut, N. Endothelial nitric oxide synthase and angiotensin converting enzyme gene polymorphisms in migraine patients. Noropsikiyatri Ars., 2013, 50(3), 274-278. https://dx.doi.org/10.4274%2Fnpa.y6665
[PMID: 28360555]
[43]
Horasanlı, B.; Ataç, F.B.; Çöven, İ.; Karakurum Goksel, B.; Benli, S. Angiotensin I-converting enzyme gene (I/D) polymorphism in patients with migraine. Headache, 2013, 53(1), 161-164.
[http://dx.doi.org/10.1111/head.12008] [PMID: 23278516]
[44]
Sipahi, T.; Güldiken, B.; Kabayel, L.; Palabiyik, O.; Özkan, H.; Kiliç, T.O.; Süt, N.; Turgut, N. Endothelial nitric oxide synthase and angiotensin converting enzyme gene polymorphisms in migraine patients., Noro Psikiyatri Arsivi, 2013, 50(3), 274-278.
[PMID: 28360555]
[45]
Goadsby, P.J. Pathophysiology of migraine. Ann. Indian Acad. Neurol., 2012, 15( 1), 15-22.
[http://dx.doi.org/10.4103/0972-2327.99993]
[46]
Gooriah, R. Evidence-based treatments for adults with migraine. Pain Res. Treat., 2015, 2015 629382
[http://dx.doi.org/10.1155/2015/629382]
[47]
Rocha, N.P.; Simoes E Silva, A.C.; Prestes, T.R.R.; Feracin, V.; Machado, C.A.; Ferreira, R.N.; Teixeira, A.L.; de Miranda, A.S. RAS in the central nervous system: Potential role in neuropsychiatric disorders. Curr. Med. Chem., 2018, 25(28), 3333-3352.
[http://dx.doi.org/10.2174/0929867325666180226102358] [PMID: 29484978]
[48]
Jackson, L.; Eldahshan, W.; Fagan, S.C.; Ergul, A. Within the brain: The renin angiotensin system. Int. J. Mol. Sci., 2018, 19(3)E876
[http://dx.doi.org/10.3390/ijms19030876] [PMID: 29543776]
[49]
Unger, T.; Steckelings, U.M.; Dzau, V.J. The Angiotensin AT2 receptor: From enigma to therapeutic target.The Protective Arm of the Renin Angiotensin System: Functional Aspects and Therapeutic Implications; Unger, T.; Steckelings, U.M.; dos Santos, R.A.S., Eds.; Academic Press: Cambridge, MA, 2015, pp. 1-9.
[50]
Bessaguet, F.; Magy, L.; Desmoulière, A.; Demiot, C. The therapeutic potential of renin angiotensin aldosterone system (RAAS) in chronic pain: from preclinical studies to clinical trials. Expert Rev. Neurother., 2016, 16(3), 331-339.
[http://dx.doi.org/10.1586/14737175.2016.1150179] [PMID: 26852820]
[51]
Marques-Lopes, J.; Pinto, M.; Pinho, D.; Morato, M.; Patinha, D.; Albino-Teixeira, A.; Tavares, I. Microinjection of angiotensin II in the caudal ventrolateral medulla induces hyperalgesia. Neuroscience, 2009, 158(4), 1301-1310.
[http://dx.doi.org/10.1016/j.neuroscience.2008.11.044] [PMID: 19116162]
[52]
Iwai, M.; Inaba, S.; Tomono, Y.; Kanno, H.; Iwanami, J.; Mogi, M.; Horiuchi, M. Attenuation of focal brain ischemia by telmisartan, an angiotensin II type 1 receptor blocker, in atherosclerotic apolipoprotein E-deficient mice. Hypertens. Res., 2008, 31(1), 161-168.
[http://dx.doi.org/10.1291/hypres.31.161] [PMID: 18360031]
[53]
Lauritzen, M.; Dreier, J.P.; Fabricius, M.; Hartings, J.A.; Graf, R.; Strong, A.J. Clinical relevance of cortical spreading depression in neurological disorders: migraine, malignant stroke, subarachnoid and intracranial hemorrhage, and traumatic brain injury. J. Cereb. Blood Flow Metab., 2011, 31(1), 17-35.
[http://dx.doi.org/10.1038/jcbfm.2010.191] [PMID: 21045864]
[54]
Onder, G.; Pahor, M.; Gambassi, G.; Federici, A.; Savo, A.; Carbonin, P.; Bernabei, R. GIFA Study. Association between ACE inhibitors use and headache caused by nitrates among hypertensive patients: Results from the Italian group of pharmacoepidemiology in the elderly (GIFA). Cephalalgia, 2003, 23(9), 901-906.
[http://dx.doi.org/10.1046/j.1468-2982.2003.00627.x] [PMID: 14616932]
[55]
Bigal, M.E.; Kurth, T.; Hu, H.; Santanello, N.; Lipton, R.B. Migraine and cardiovascular disease: possible mechanisms of interaction. Neurology, 2009, 72(21), 1864-1871.
[http://dx.doi.org/10.1212/WNL.0b013e3181a71220] [PMID: 19470970]
[56]
Mahmoud, A.N.; Mentias, A.; Elgendy, A.Y.; Qazi, A.; Barakat, A.F.; Saad, M.; Mohsen, A.; Abuzaid, A.; Mansoor, H.; Mojadidi, M.K.; Elgendy, I.Y. Migraine and the risk of cardiovascular and cerebrovascular events: a meta-analysis of 16 cohort studies including 1 152 407 subjects. BMJ Open, 2018, 8(3), e020498-e020498.
[http://dx.doi.org/10.1136/bmjopen-2017-020498] [PMID: 29593023]
[57]
Bond, D.S.; Roth, J.; Nash, J.M.; Wing, R.R. Migraine and obesity: epidemiology, possible mechanisms and the potential role of weight loss treatment. Obes. Rev., 2011, 12(5), e362-e371.
[http://dx.doi.org/10.1111/j.1467-789X.2010.00791.x] [PMID: 20673279]
[58]
Rammohan, K.; Mundayadan, S.M.; Das, S.; Shaji, C.V. Migraine and mood disorders: Prevalence, clinical correlations and disability. J. Neurosci. Rural Pract., 2019, 10(1), 28-33.
[http://dx.doi.org/10.4103/jnrp.jnrp_146_18] [PMID: 30765967]


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Article Details

VOLUME: 27
ISSUE: 6
Year: 2020
Published on: 09 June, 2020
Page: [512 - 519]
Pages: 8
DOI: 10.2174/0929866527666200129160136
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