Beyond chronic migraine: a systematic review and expert opinion on the off-label use of botulinum neurotoxin type-A in other primary headache disorders

References

• Headache Classification Committee of the International Headache Society (IHS). Headache Classification Committee of the International Headache Society (IHS) The International Classification of Headache Disorders, 3rd edition. Cephalalgia. 2018;38(1):1–211.
   PubMed Web of Science ®Google Scholar
• Mier RW, Primary Headaches DS. Dent Clin North Am. 2018;62(4):611–628.
   Google Scholar
• GBD 2016. Headache Collaborators. Global, regional, and national burden of migraine and tension-type headache, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol. 2018;17(11):954–976.
   PubMed Web of Science ®Google Scholar
• GBD 2016. Disease and Injury Incidence and Prevalence Collaborators. Global, regional, and national incidence, prevalence, and years lived with disability for 328 diseases and injuries for 195 countries, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet. 2017;390(10100):1211–1259.
   PubMed Web of Science ®Google Scholar
• Ford JH, Nero D, Kim G, et al. Societal burden of cluster headache in the United States: a descriptive economic analysis. J Med Econ. 2018;21(1):107–111.
   PubMed Web of Science ®Google Scholar
• Ashina S, Mitsikostas DD, Lee MJ, et al. Tension-type headache. Nat Rev Dis Primers. 2021;7(1):24.
   PubMed Web of Science ®Google Scholar
• Argyriou AA, Vikelis M, Mantovani E, et al. Recently available and emerging therapeutic strategies for the acute and prophylactic management of cluster headache: a systematic review and expert opinion. Expert Rev Neurother. 2021;21(2):235–248.
   PubMed Web of Science ®Google Scholar
• Ashina M, Buse DC, Ashina H, et al. Migraine: integrated approaches to clinical management and emerging treatments. Lancet. 2021;397(10283):1505–1518.
   PubMed Web of Science ®Google Scholar
• Pirazzini M, Rossetto O, Eleopra R, et al. Toxicology. Pharmacol Rev. 2017;69(2):200–235.
   PubMed Web of Science ®Google Scholar
• Frampton JE. OnabotulinumtoxinA in Chronic Migraine: a Profile of Its Use. CNS Drugs. 2020;34(12):1287–1298.
   PubMed Web of Science ®Google Scholar
• Abrams SB, Hallett M. Clinical utility of different botulinum neurotoxin preparations. Toxicon. 2013;67:81–86.
   PubMed Web of Science ®Google Scholar
• Vikelis M, Argyriou AA, Dermitzakis EV, et al. Onabotulinumtoxin-A treatment in Greek patients with chronic migraine. J Headache Pain. 2016;17(1):84.
   PubMedGoogle Scholar
• Vikelis M, Argyriou AA, Dermitzakis EV, et al. Sustained onabotulinumtoxinA therapeutic benefits in patients with chronic migraine over 3 years of treatment. J Headache Pain. 2018;19(1):87.
   PubMed Web of Science ®Google Scholar
• Bendtsen L, Zakrzewska JM, Abbott J, et al. European Academy of Neurology guideline on trigeminal neuralgia. Eur J Neurol. 2019;26(6):831–849.
   PubMed Web of Science ®Google Scholar
• Sandrini G, De Icco R, Tassorelli C, et al. Botulinum neurotoxin type A for the treatment of pain: not just in migraine and trigeminal neuralgia. J Headache Pain. 2017;18(1):38.
   PubMedGoogle Scholar
• Schueler M, Messlinger K, Dux M, et al. Extracranial projections of meningeal afferents and their impact on meningeal nociception and headache. Pain. 2013;154(9):1622–1631.
   PubMed Web of Science ®Google Scholar
• Burstein R, Blake P, Schain A, et al. Extracranial origin of headache. Curr Opin Neurol. 2017;30(3):263–271.
   PubMed Web of Science ®Google Scholar
• Zhang X, Strassman AM, Novack V, et al. 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):875–886.
   PubMed Web of Science ®Google Scholar
• Melo-Carrillo A, Strassman AM, Nir -R-R, et al. Fremanezumab—A Humanized Monoclonal Anti-CGRP Antibody—Inhibits Thinly Myelinated (Aδ) But Not Unmyelinated (C) Meningeal Nociceptors. J Neurosci. 2017;37(44):10587–10596.
   PubMed Web of Science ®Google Scholar
• Pellesi L, Do TP, Ashina H, et al. Dual Therapy With Anti-CGRP Monoclonal Antibodies and Botulinum Toxin for Migraine Prevention: is There a Rationale? Headache. 2020;60(6):1056–1065.
   PubMed Web of Science ®Google Scholar
• Edvinsson JCA, Warfvinge K, Krause DN, et al., C-fibers may modulate adjacenAδ-fibers through axon-axon CGRP signaling at nodes of Ranvier in the trigeminal system. J Headache Pain. 20(1): 105. 2019. .
   PubMed Web of Science ®Google Scholar
• Antonucci F, Rossi C, Gianfranceschi L, et al. Long-distance retrograde effects of botulinum neurotoxin A. J Neurosci. 2008;28(14):3689‐3696.
   PubMed Web of Science ®Google Scholar
• Restani L, Novelli E, Bottari D, et al. Botulinum neurotoxin A impairs neurotransmission following retrograde transynaptic transport. Traffic. 2012;13(8):1083‐1089.
   PubMed Web of Science ®Google Scholar
• Martinelli D, Arceri S, Tronconi L, et al. Chronic migraine and botulinum toxin type a: where do paths cross? Toxicon. 2020;178:69–76.
   PubMed Web of Science ®Google Scholar
• Huang P, Khan I, Suhail M, et al. Spinal botulinum neurotoxin B: effects on afferent transmitter release and nociceptive processing. PLoS One. 2011;6(4):e19126.
   PubMed Web of Science ®Google Scholar
• Coelho A, Oliveira R, Rossetto O, et al. Intrathecal administration of botulinum toxin type A improves urinary bladder function and reduces pain in rats with cystitis. Eur J Pain. 2014;18(10):1480‐1489.
   Web of Science ®Google Scholar
• Cernuda-Morollón E, Ramón C, Martínez-Camblor P, et al. OnabotulinumtoxinA decreases interictal CGRP plasma levels in patients with chronic migraine. Pain. 2015;156(5):820–824.
   PubMed Web of Science ®Google Scholar
• Kim D-W, Lee S-K, Ahnn J. Botulinum toxin as a pain killer: players and actions in antinociception. Toxins (Basel). 2015;7(7):2435–2453.
   PubMed Web of Science ®Google Scholar
• Aoki KR. Evidence for antinociceptive activity of botulinum toxin type A in pain management. Headache. 2003;43(suppl s1):S9–S15.
   PubMedGoogle Scholar
• Burstein R, Blumenfeld AM, Silberstein SD, et al. Mechanism of action of onabotulinumtoxina in chronic migraine: a narrative review. Headache. 2020;60(7):1259–1272.
   PubMed Web of Science ®Google Scholar
• Zychowska M, Rojewska E, Makuch W, et al. Participation of pro- and anti-nociceptive interleukins in botulinum toxin A-induced analgesia in a rat model of neuropathic pain. Eur J Pharmacol. 2016;791:377–388.
   PubMed Web of Science ®Google Scholar
• Diener HC, Dodick DW, Aurora SK, et al. PREEMPT 2 chronic migraine study group. 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.
   PubMed Web of Science ®Google Scholar
• Aurora SK, Dodick DW, Turkel CC, et al. PREEMPT 1 chronic migraine study group. 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.
   PubMed Web of Science ®Google Scholar
• Dodick DW, Turkel CC, DeGryse RE, et al. PREEMPT chronic migraine study group. onabotulinumtoxinA for treatment of chronic migraine: pooled results from the double-blind, randomized, placebo-controlled phases of the PREEMPT clinical program. Headache. 2010;50(6):921–936.
   PubMed Web of Science ®Google Scholar
• Barbanti P, Ferroni P. Onabotulinum toxin A in the treatment of chronic migraine: patient selection and special considerations. J Pain Res. 2017;10:2319–2329.
   PubMed Web of Science ®Google Scholar
• Aurora SK, Dodick DW, Diener HC, et al. OnabotulinumtoxinA for chronic migraine: efficacy, safety, and tolerability in patients who received all five treatment cycles in the PREEMPT clinical program. Acta Neurol Scand. 2014;129(1):61–70.
   PubMed Web of Science ®Google Scholar
• Silberstein SD, Dodick DW, Aurora SK, et al. Per cent of patients with chronic migraine who responded per onabotulinumtoxinA treatment cycle: PREEMPT. J Neurol Neurosurg Psychiatry. 2015;86(9):996–1001.
   PubMed Web of Science ®Google Scholar
• Wiener PK, Blumenfeld AM, Eross EJ, et al. Long-term safety and tolerability of onabotulinumtoxina treatment in patients with chronic migraine: results of the COMPEL study. Drug Saf. 2019;42(8):1013–1024.
   PubMed Web of Science ®Google Scholar
• Moher D, Shamseer L, Clarke M, et al. PRISMA-P Group. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev. 2015;4(1):1.
   PubMed Web of Science ®Google Scholar
• Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71.
   PubMed Web of Science ®Google Scholar
• Higgins JPT, Thomas J, Chandler J, et al. Cochrane handbook for systematic reviews of interventions. 2nd Edition. Chichester (UK): John Wiley & Sons;2019. (editors). Available from. www.training.cochrane.org/handbook
   Google Scholar
• Ouzzani M, Hammady H, Fedorowicz Z, et al. Rayyan-a web and mobile app for systematic reviews. Syst Rev. 2016;5(1):210.
   PubMedGoogle Scholar
• Oxford Centre for Evidence-Based Medicine Levels of Evidence Working Group. OECBM levels of evidence system. [cited 2021 Jul 10]. Available from (https://www.cebm.ox.ac.uk/resources/levels-of-evidence/oxford-centre-for-evidence-based-medicine-levels-of-evidence-march-2009)
   Google Scholar
• Eross EJ, Gladstone JP, Lewis S, et al. Duration of migraine is a predictor for response to botulinum toxin type A. Headache. 2005;45(4):308–314.
   PubMed Web of Science ®Google Scholar
• Elkind AH, O’Carroll P, Blumenfeld A, et al. BoNTA-024-026-036 study group. A series of three sequential, randomized, controlled studies of repeated treatments with botulinum toxin type A for migraine prophylaxis. J Pain. 2006;7(10):688–696.
   PubMed Web of Science ®Google Scholar
• Jakubowski M, McAllister PJ, Bajwa ZH, et al. Exploding vs. imploding headache in migraine prophylaxis with botulinum toxin A. Pain. 2006;125(3):286–295.
   PubMed Web of Science ®Google Scholar
• Aurora SK, Gawel M, Brandes JL, et al. BOTOX North American episodic migraine study group. botulinum toxin type a prophylactic treatment of episodic migraine: a randomized, double-blind, placebo-controlled exploratory study. Headache. 2007;47(4):486–499.
   PubMed Web of Science ®Google Scholar
• Relja M, Poole AC, Schoenen J, et al. European BoNTA headache study group. A double-blind, randomized, placebo-controlled, parallel group study of multiple treatments of botulinum toxin type A (BoNTA) for the prophylaxis of episodic migraine headaches. Cephalalgia. 2007;27(6):492–503.
   PubMed Web of Science ®Google Scholar
• Saper JR, Mathew NT, Loder EW, et al. BoNTA-009 study group. A double-blind, randomized, placebo-controlled comparison of botulinum toxin type a injection sites and doses in the prevention of episodic migraine. Pain Med. 2007;8(6):478–485.
   PubMed Web of Science ®Google Scholar
• Kim CC, Bogart MM, Wee SA, et al. Predicting migraine responsiveness to botulinum toxin type A injections. Arch Dermatol. 2010;146(2):159–163.
   PubMedGoogle Scholar
• Chitsaz A, Ghorbani A, Hoseinzadeh H, et al. Comparison of botulinum toxin type-A and divalproex sodium for prevention of chronic and episodic migraine. Neurol Asia. 2012;17(2):127–132.
   Web of Science ®Google Scholar
• Velasco-Juanes F, Gomez-Esteban JC, Fernandez-Valle T, et al. Clinical treatment of chronic and episodic migraine with onabotulinumtoxinA in a real-world setting. Drugs Ther Perspect. 2018;34:335–343.
   Google Scholar
• Alpuente A, Gallardo VJ, Torres-Ferrus M, et al. Early efficacy and late gain in chronic and high-frequency episodic migraine with onabotulinumtoxinA. Eur J Neurol. 2019;26(12):1464–1470.
   PubMed Web of Science ®Google Scholar
• Smuts JA, Baker MK, Smuts HM, et al. Prophylactic treatment of chronic tension-type headache using botulinum toxin A. Eur J Neurol. 1999;6(Supp 4):S99–S102.
   PubMedGoogle Scholar
• Rollnik JD, Tanneberger O, Schubert M, et al. Treatment of tension-type headache with botulinum toxin type A: a double-blind, placebo-controlled study. Headache. 2000;40(4):300–305.
   PubMed Web of Science ®Google Scholar
• Schmitt WH, Slowey E, Fravi N, et al. Effect of botulinum toxin A injections in the treatment of chronic tension-type headache: a double-blind, placebo-controlled trial. Headache. 2001;41(7):658–664.
   PubMed Web of Science ®Google Scholar
• Padberg M, de Bruijn SF, de Haan RJ, et al. Treatment of chronic tension-type headache with botulinum toxin: a double-blind, placebo-controlled clinical trial. Cephalalgia. 2004;24(8):675–680.
   PubMed Web of Science ®Google Scholar
• Relja M, Telarović S. Botulinum toxin in tension-type headache. J Neurol. 2004;251(Suppl 1):I12–4.
   PubMedGoogle Scholar
• Schulte-Mattler WJ, Krack P. BoNTTH study group. treatment of chronic tension-type headache with botulinum toxin A: a randomized, double-blind, placebo-controlled multicenter study. Pain. 2004;109(1–2):110–114.
   PubMed Web of Science ®Google Scholar
• Silberstein SD, Göbel H, Jensen R, et al. Botulinum toxin type A in the prophylactic treatment of chronic tension-type headache: a multicentre, double-blind, randomized, placebo-controlled, parallel-group study. Cephalalgia. 2006;26(7):790–800.
   PubMed Web of Science ®Google Scholar
• Erdemoglu AK, Varlibas A. The long-term efficacy and safety of botulinum toxin in refractory chronic tension-type headache. J Headache Pain. 2007;8(5):294–300.
   PubMedGoogle Scholar
• Straube A, Empl M, Ceballos-Baumann A, et al. Dysport tension-type headache study group. pericranial injection of botulinum toxin type A (Dysport) for tension-type headache - a multicentre, double-blind, randomized, placebo-controlled study. Eur J Neurol. 2008;15(3):205–213.
   PubMed Web of Science ®Google Scholar
• Hamdy SM, Samir H, El-Sayed M, et al. Botulinum toxin: could it be an effective treatment for chronic tension-type headache? J Headache Pain. 2009;10(1):27–34.
   PubMed Web of Science ®Google Scholar
• Harden RN, Cottrill J, Gagnon CM, et al. Botulinum toxin a in the treatment of chronic tension-type headache with cervical myofascial trigger points: a randomized, double-blind, placebo-controlled pilot study. Headache. 2009;49(5):732–743.
   PubMed Web of Science ®Google Scholar
• Sostak P, Krause P, Förderreuther S, et al. Botulinum toxin type-A therapy in cluster headache: an open study. J Headache Pain. 2007;8(4):236–241.
   PubMed Web of Science ®Google Scholar
• Bratbak DF, Nordgård S, Stovner LJ, et al. Pilot study of sphenopalatine injection of onabotulinumtoxinA for the treatment of intractable chronic cluster headache. Cephalalgia. 2016;36(6):503–509.
   PubMed Web of Science ®Google Scholar
• Aschehoug I, Bratbak DF, Tronvik EA. Long-term outcome of patients with intractable chronic cluster headache treated with injection of onabotulinum toxin a toward the sphenopalatine ganglion - an observational study. Headache. 2018;58(10):1519–1529.
   PubMed Web of Science ®Google Scholar
• Lampl C, Rudolph M, Bräutigam E. OnabotulinumtoxinA in the treatment of refractory chronic cluster headache. J Headache Pain. 2018;19(1):45.
   PubMedGoogle Scholar
• Crespi J, Bratbak D, Dodick DW, et al. Open-label, multi-dose, pilot safety study of injection of onabotulinumtoxina toward the otic ganglion for the treatment of intractable chronic cluster headache. Headache. 2020;60(8):1632–1643.
   PubMed Web of Science ®Google Scholar
• Zabalza RJ. Sustained response to botulinum toxin in SUNCT syndrome. Cephalalgia. 2012;32(11):869–872.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Chen Y, Lian Y. Sustained response to botulinum toxin type A in SUNA syndrome. Pain Med. 2019;20(2):419–421.
   PubMed Web of Science ®Google Scholar
• Garza I, Cutrer FM. Pain relief and persistence of dysautonomic features in a patient with hemicrania continua responsive to botulinum toxin type A. Cephalalgia. 2010;30(4):500–503.
   PubMed Web of Science ®Google Scholar
• Miller S, Correia F, Lagrata S, et al. OnabotulinumtoxinA for hemicrania continua: open label experience in 9 patients. J Headache Pain. 2015;16:19.
   PubMed Web of Science ®Google Scholar
• Piovesan EJ, Teive HG, Kowacs PA, et al. Botulinum neurotoxin type-A for primary stabbing headache. An open study. Arq Neuropsiquiatr. 2010;68(2):212–215.
   PubMed Web of Science ®Google Scholar
• Mathew NT, Kailasam J, Meadors L. Botulinum toxin type A for the treatment of nummular headache: four case studies. Headache. 2008;48(3):442–447.
   PubMed Web of Science ®Google Scholar
• García-Azorín D, Trigo-López J, Á S, et al. Observational, open-label, non-randomized study on the efficacy of onabotulinumtoxinA in the treatment of nummular headache: the pre-numabot study. Cephalalgia. 2019;39(14):1818–1826.
   PubMed Web of Science ®Google Scholar
• Gutiérrez-Sánchez M, García-Azorín D, Á G-V, et al. Paroxysmal headache with extracephalic irradiation: proposal for a new variant of epicrania fugax in a series of five patients. Cephalalgia. 2020;40(9):959–965.
   PubMed Web of Science ®Google Scholar
• Chavarría-Miranda A, ÁL G, Talavera B, et al. Linear headache: a novel entity or a variant of nummular headache? Clinical characteristics and treatment response in a series of 16 patients. Pain Med. 2021 Mar 16. pnaa436.
   PubMed Web of Science ®Google Scholar
• Marziniak M, Voss J, Evers S. Hypnic headache successfully treated with botulinum toxin type A. Cephalalgia. 2007;27(9):1082–1084.
   PubMed Web of Science ®Google Scholar
• Ali A, Kriegler J, Tepper S, et al. New daily persistent headache and onabotulinumtoxina therapy. Clin Neuropharmacol. 2019;42(1):1–3.
   PubMed Web of Science ®Google Scholar
• Botulinum Toxin Type A Block of the Otic Ganglion in Chronic Cluster Headache: Safety Issues – full text view - clinicaltrials.gov. [cited 2021 May 10]. Available from: https://clinicaltrials.gov/ct2/show/NCT03066635
   Google Scholar
• Botulinum Toxin Type A Blockade of the Sphenopalatine Ganglion in Treatment-refractory Chronic Cluster Headache (BASIC) – full text view - clinicaltrials.gov. [cited 2021 May 10]. Available from: https://clinicaltrials.gov/ct2/show/NCT03944876
   Google Scholar
• Botulinum Toxin A in frequent and chronic Tension-type headache (BACT) – full text view - clinicaltrials.gov. [cited 2021 May 10]. Available from: https://clinicaltrials.gov/ct2/show/NCT04857671
   Google Scholar
• Castelnuovo G, Giusti EM, Manzoni GM, et al. What is the role of the placebo effect for pain relief in neurorehabilitation? clinical implications from the italian consensus conference on pain in neurorehabilitation. Front Neurol. [2018 May];18(9):310.
   Google Scholar
• DB S, Benedetti F, MFP P. Different routes of administration in chronic migraine prevention lead to different placebo responses: a meta-analysis. Pain. 2021 Jun 14. Online ahead of print. https://doi.org/10.1097/j.pain.0000000000002365
   Google Scholar
• Mitsikostas DD, Blease C, Carlino E, et al. European headache federation. european headache federation recommendations for placebo and nocebo terminology. J Headache Pain. 2020 Sep 25;21(1):117.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• de Tommaso M, Tension Type F-D-L-PC. Headache. Curr Rheumatol Rev. 2016;12(2):127–139.
   PubMed Web of Science ®Google Scholar
• Fernández-De-Las-Peñas C, Arendt-Nielsen L. Improving understanding of trigger points and widespread pressure pain sensitivity in tension-type headache patients: clinical implications. Expert Rev Neurother. 2017;17(9):933–939.
   PubMed Web of Science ®Google Scholar
• Domínguez C, Pozo-Rosich P, Torres-Ferrús M, et al. Onabotulinumtoxin A in chronic migraine: predictors of response. A prospective multicentre descriptive study. Eur J Neurol. 2018;25:411–416.
   PubMed Web of Science ®Google Scholar
• Torres-Ferrús M, Quintana M, Fernandez-Morales J, et al. When does chronic migraine strike? A clinical comparison of migraine according to the headache days suffered per month. Cephalalgia. 2017;37(2):104–113.
   PubMed Web of Science ®Google Scholar
• Torres-Ferrús M, Ursitti F, Alpuente A, et al. School of advanced studies of european headache federation (EHF-SAS). From transformation to chronification of migraine: pathophysiological and clinical aspects. J Headache Pain. 2020;21(1):42.
   PubMed Web of Science ®Google Scholar
• Durham PL, Cady R. Insights into the mechanism of onabotulinumtoxinA in chronic migraine. Headache. 2011;51(10):1573–1577.
   PubMed Web of Science ®Google Scholar