116
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Amplification of Glyceryl Trinitrate-Induced Headache Features By Noxious Craniofacial Stimuli in Pain-Free Healthy Humans

, , , , , & show all
Pages 17-35 | Received 24 Aug 2018, Accepted 17 Sep 2018, Published online: 03 Dec 2018

References

  • Murrell W . Nitro-glycerine as a remedy for angina pectoris . Lancet1 , 80 – 81 ; 113-ll115,151–152,225–227 ( 1879 ).
  • Horwitz LD , HermanMV , GorlinR . Clinical response to nitroglycerin as a diagnostic test for coronary-artery disease . Am. J. Cardiol.29 ( 2 ), 149 – 153 ( 1972 ).
  • Hsi DH , RoshandelA , SinghN , SzombathyT , MeszarosZS . Headache response to glyceryl trinitrate in patients with and without obstructive coronary artery disease . Heart91 ( 9 ), 1164 – 1166 ( 2005 ).
  • Iversen HK , ThomsenLL . Nitroglycerin-induced headache – an experimental human headache model . Fr. Head. Res.5 , 251 – 258 ( 1995 ).
  • Ashina M , HansenJM , BoAD , OlesenJ . Human models of migraine – short-term pain for long-term gain . Nat. Rev. Neurol.13 ( 12 ), 713 – 724 ( 2017 ).
  • Holthusen H , ArndtJO . Nitric-oxide evokes pain at nociceptors of the paravascular tissue and veins in humans . J. Physiol.487 ( 1 ), 253 – 258 ( 1995 ).
  • Van Der Kuy PH , LohmanJJ . The role of nitric oxide in vascular headache . Pharm. World. Sci.25 ( 4 ), 146 – 151 ( 2003 ).
  • Olesen J , ThomsenLL , IversenH . Nitric-oxide is a key molecule in migraine and other vascular headaches . Trends Pharmacol. Sci.15 ( 5 ), 149 – 153 ( 1994 ).
  • Thomsen LL , KruuseC , IversenHK , OlesenJ . A nitric oxide donor (nitroglycerin) triggers genuine migraine attacks . Eur. J. Neurol.1 ( 1 ), 73 – 80 ( 1994 ).
  • Olesen J , Jansen-OlesenI . Towards a reliable animal model of migraine . Cephalalgia32 ( 7 ), 578 – 580 ( 2012 ).
  • Christiansen I , ThomsenLL , DaugaardD , UlrichV , OlesenJ . Glyceryl trinitrate induces attacks of migraine without aura in sufferers of migraine with aura . Cephalalgia19 ( 7 ), 660 – 667 ; discussion 626 ( 1999 ).
  • Christiansen I , DaugaardD , Lykke ThomsenL , OlesenJ . Glyceryl trinitrate induced headache in migraineurs – relation to attack frequency . Eur. J. Neurol.7 ( 4 ), 405 – 411 ( 2000 ).
  • Olesen J , ThomsenLL , LassenLH , OlesenIJ . The nitric oxide hypothesis of migraine and other vascular headaches . Cephalalgia15 ( 2 ), 94 – 100 ( 1995 ).
  • Neri M , FrustaciA , MilicMet al. A meta-analysis of biomarkers related to oxidative stress and nitric oxide pathway in migraine . Cephalalgia35 ( 10 ), 931 – 937 ( 2015 ).
  • Olesen J , IversenHK , ThomsenLL . Nitric oxide supersensitivity: a possible molecular mechanism of migraine pain . Neuroreport4 ( 8 ), 1027 – 1030 ( 1993 ).
  • Bagdy G , RibaP , KecskemetiV , ChaseD , JuhaszG . Headache-type adverse effects of NO donors: vasodilation and beyond . Brit. J. Pharmacol.160 ( 1 ), 20 – 35 ( 2010 ).
  • Thomsen LL , OlesenJ . A pivotal role of nitric oxide in migraine pain . Ann. N. Y. Acad. Sci.835 , 363 – 372 ( 1997 ).
  • Thomsen LL , IversenHK , BrinckTA , OlesenJ . Arterial supersensitivity to nitric-oxide (nitroglycerin) in migraine sufferers . Cephalalgia13 ( 6 ), 395 – 399 ( 1993 ).
  • Messlinger K . Migraine: where and how does the pain originate?Exp. Brain Res.196 ( 1 ), 179 – 193 ( 2009 ).
  • Goadsby PJ . Pathophysiology of migraine . Ann. Indian Acad. Neur.15 , 15 – 22 ( 2012 ).
  • Ashina M , BendtsenL , JensenR , OlesenJ . Nitric oxide-induced headache in patients with chronic tension-type headache . Brain123 ( Pt 9 ), 1830 – 1837 ( 2000 ).
  • Aurora SK , WilkinsonF . The brain is hyperexcitable in migraine . Cephalalgia27 ( 12 ), 1442 – 1453 ( 2007 ).
  • Sand T , ZhitniyN , NilsenKB , HeldeG , HagenK , StovnerLJ . Thermal pain thresholds are decreased in the migraine preattack phase . Eur. J. Neurol.15 ( 11 ), 1199 – 1205 ( 2008 ).
  • Fernandez-De-Las-Penas C , MadeleineP , CuadradoML , GeHY , Arendt-NielsenL , ParejaJA . Pressure pain sensitivity mapping of the temporalis muscle revealed bilateral pressure hyperalgesia in patients with strictly unilateral migraine . Cephalalgia29 ( 6 ), 670 – 676 ( 2009 ).
  • Aurora SK , BrinMF . Chronic migraine: an update on physiology, imaging, and the mechanism of action of two available pharmacologic therapies . Headache57 ( 1 ), 109 – 125 ( 2017 ).
  • Burstein R , YarnitskyD , Goor-AryehI , RansilBJ , BajwaZH . An association between migraine and cutaneous allodynia . Ann. Neurol.47 ( 5 ), 614 – 624 ( 2000 ).
  • Burstein R , NosedaR , BorsookD . Migraine: multiple processes, complex pathophysiology . J. Neurosci.35 ( 17 ), 6619 – 6629 ( 2015 ).
  • Brennan KC , PietrobonD . A systems neuroscience approach to migraine . Neuron97 ( 5 ), 1004 – 1021 ( 2018 ).
  • Gazerani P , AndersenOK , Arendt-NielsenL . A human experimental capsaicin model for trigeminal sensitization. Gender-specific differences . Pain118 ( 1–2 ), 155 – 163 ( 2005 ).
  • Gazerani P , Arendt-NielsenL . The impact of ethnic differences in response to capsaicin-induced trigeminal sensitization . Pain117 ( 1–2 ), 223 – 229 ( 2005 ).
  • Oono Y , WangK , SvenssonP , Arendt-NielsenL . Conditioned pain modulation evoked by different intensities of mechanical stimuli applied to the craniofacial region in healthy men and women . J. Orofac. Pain25 ( 4 ), 364 – 375 ( 2011 ).
  • Oono Y , Baad-HansenL , WangK , Arendt-NielsenL , SvenssonP . Effect of conditioned pain modulation on trigeminal somatosensory function evaluated by quantitative sensory testing . Pain154 ( 12 ), 2684 – 2690 ( 2013 ).
  • World Medical A . World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects . JAMA310 ( 20 ), 2191 – 2194 ( 2013 ).
  • Perrotta A , SerraoM , TassorelliCet al. Oral nitric-oxide donor glyceryl-trinitrate induces sensitization in spinal cord pain processing in migraineurs: a double-blind, placebo-controlled, cross-over study . Eur. J. Pain15 ( 5 ), 482 – 490 ( 2011 ).
  • Antonaci F , BovimG , FasanoML , BonamicoL , ShenJM . Pain threshold in humans. A study with the pressure algometer . Funct. Neurol.7 ( 4 ), 283 – 288 ( 1992 ).
  • Fischer AA . Pressure algometry over normal muscles. Standard values, validity and reproducibility of pressure threshold . Pain30 ( 1 ), 115 – 126 ( 1987 ).
  • Du Jardin KG , GregersenLS , RoslandTet al. Assessment of pain response in capsaicin-induced dynamic mechanical allodynia using a novel and fully automated brushing device . Pain Res. Manag.18 ( 1 ), 6 – 10 ( 2013 ).
  • Gazerani P , AndersenOK , Arendt-NielsenL . Site-specific, dose-dependent, and sex-related responses to the experimental pain model induced by intradermal injection of capsaicin to the foreheads and forearms of healthy humans . J. Orofac. Pain21 ( 4 ), 289 – 302 ( 2007 ).
  • Roberts K , ShenoyR , AnandP . A novel human volunteer pain model using contact heat evoked potentials (CHEP) following topical skin application of transient receptor potential agonists capsaicin, menthol and cinnamaldehyde . J. Clin. Neurosci.18 ( 7 ), 926 – 932 ( 2011 ).
  • Zheng Z , GibsonSJ , HelmeRD , McmeekenJM . The effect of local anaesthetic on age-related capsaicin-induced mechanical hyperalgesia – a randomised, controlled study . Pain144 ( 1–2 ), 101 – 109 ( 2009 ).
  • Melzack R . The McGill Pain Questionnaire: major properties and scoring methods . Pain1 ( 3 ), 277 – 299 ( 1975 ).
  • Iversen HK , OlesenJ . Headache induced by a nitric oxide donor (nitroglycerin) responds to sumatriptan. A human model for development of migraine drugs . Cephalalgia16 ( 6 ), 412 – 418 ( 1996 ).
  • Fullerton T , Komorowski-SwiatekD , ForrestA , GengoFM . The pharmacodynamics of sumatriptan in nitroglycerin-induced headache . J. Clin. Pharmacol.39 ( 1 ), 17 – 29 ( 1999 ).
  • Cairns BE , HuJW , Arendt-NielsenL , SessleBJ , SvenssonP . Sex-related differences in human pain and rat afferent discharge evoked by injection of glutamate into the masseter muscle . J. Neurophysiol.86 ( 2 ), 782 – 791 ( 2001 ).
  • Erdener SE , DalkaraT . Modelling headache and migraine and its pharmacological manipulation . Br. J. Pharmacol.171 ( 20 ), 4575 – 4594 ( 2014 ).
  • Bednarczyk EM , WackDS , KassabMYet al. Brain blood flow in the nitroglycerin (GTN) model of migraine: measurement using positron emission tomography and transcranial Doppler . Cephalalgia22 ( 9 ), 749 – 757 ( 2002 ).
  • Ashina M , HansenJM , OlesenJ . Pearls and pitfalls in human pharmacological models of migraine: 30 years’ experience . Cephalalgia33 ( 8 ), 540 – 553 ( 2013 ).
  • Iversen HK , OlesenJ , TfelthansenP . Intravenous nitroglycerin as an experimental-model of vascular headache – basic characteristics . Pain38 ( 1 ), 17 – 24 ( 1989 ).
  • Iversen HK , OlesenJ . Nitroglycerin-induced headache is not dependent on histamine-release – support for a direct nociceptive action of nitric-oxide . Cephalalgia14 ( 6 ), 437 – 442 ( 1994 ).
  • Iversen HK . Human migraine models . Cephalalgia21 ( 7 ), 781 – 785 ( 2001 ).
  • Juhasz G , ZsombokT , JakabB , NemethJ , SzolcsanyiJ , BagdyG . Sumatriptan causes parallel decrease in plasma calcitonin gene-related peptide (CGRP) concentration and migraine headache during nitroglycerin induced migraine attack . Cephalalgia25 ( 3 ), 179 – 183 ( 2005 ).
  • Tvedskov JF , ThomsenLL , ThomsenLLet al. The effect of propranolol on glyceryltrinitrate-induced headache and arterial response . Cephalalgia24 ( 12 ), 1076 – 1087 ( 2004 ).
  • Tvedskov JF , ThomsenLL , IversenHK , GibsonA , WiliamsP , OlesenJ . The prophylactic effect of valproate on glyceryltrinitrate induced migraine . Cephalalgia24 ( 7 ), 576 – 585 ( 2004 ).
  • Akerman S , WilliamsonDJ , KaubeH , GoadsbyPJ . The effect of anti-migraine compounds on nitric oxide-induced dilation of dural meningeal vessels . Eur. J. Pharmacol.452 ( 2 ), 223 – 228 ( 2002 ).
  • Strecker T , DuxM , MesslingerK . Nitric oxide releases calcitonin-gene-related peptide from rat dura mater encephali promoting increases in meningeal blood flow . J. Vasc. Res.39 ( 6 ), 489 – 496 ( 2002 ).
  • Gozalov A , Jansen-OlesenI , KlaerkeD , OlesenJ . Role of BK(Ca) channels in cephalic vasodilation induced by CGRP, NO and transcranial electrical stimulation in the rat . Cephalalgia27 ( 10 ), 1120 – 1127 ( 2007 ).
  • Reuter U , BolayH , Jansen-OlesenIet al. Delayed inflammation in rat meninges: implications for migraine pathophysiology . Brain124 , 2490 – 2502 ( 2001 ).
  • Galeotti N , GhelardiniC . Inhibition of the PKCγ-epsilon pathway relieves from meningeal nociception in an animal model: an innovative perspective for migraine therapy?Neurotherapeutics10 ( 2 ), 329 – 339 ( 2013 ).
  • Kim GM , JinKS , ChungCS . Differential effects of corticosteroids on the expression of cyclooxygenase-2, tumour necrosis factor-α and matrix metalloproteinase-9 in an animal model of migraine . Cephalalgia28 ( 11 ), 1179 – 1187 ( 2008 ).
  • Krymchantowski A , BarbosaJS , CvaigmanM , LorenzattoW , SilvaMT . Helmet-related, external compression headache among police officers in Rio de Janeiro . Med. Gen. Med6 ( 2 ), 45 ( 2004 ).
  • Rahmani Z , KochanekA , AstrupJJ , PoulsenJN , GazeraniP . Helmet-induced headache among Danish military personnel . Scand. J. Public. Health45 ( 8 ), 818 – 823 ( 2017 ).
  • Krymchantowski AV . Headaches due to external compression . Curr. Pain. Headache Rep.14 ( 4 ), 321 – 324 ( 2010 ).
  • Bartsch T , GoadsbyPJ . Stimulation of the greater occipital nerve induces increased central excitability of dural afferent input . Brain125 , 1496 – 1509 ( 2002 ).
  • Sessle BJ , HuJW , AmanoN , ZhongG . Convergence of cutaneous, tooth pulp, visceral, neck and muscle afferents onto nociceptive and non-nociceptive neurones in trigeminal subnucleus caudalis (medullary dorsal horn) and its implications for referred pain . Pain27 ( 2 ), 219 – 235 ( 1986 ).
  • Sokolov AY , LyubashinaOA , PanteleevSS . Spinal trigeminal neurons demonstrate an increase in responses to dural electrical stimulation in the orofacial formalin test . J. Headache Pain13 ( 1 ), 75 – 82 ( 2012 ).
  • Hu JW , SessleBJ , RaboissonP , DallelR , WodaA . Stimulation of craniofacial muscle afferents induces prolonged facilitatory effects in trigeminal nociceptive brain-stem neurones . Pain48 ( 1 ), 53 – 60 ( 1992 ).
  • Yu XM , SessleBJ , HuJW . Differential effects of cutaneous and deep application of inflammatory irritant on mechanoreceptive field properties of trigeminal brain stem nociceptive neurons . J. Neurophysiol.70 ( 4 ), 1704 – 1707 ( 1993 ).
  • Lambert GA , DonaldsonC , BoersPM , ZagamiAS . Activation of trigeminovascular neurons by glyceryl trinitrate . Brain Res.887 ( 1 ), 203 – 210 ( 2000 ).
  • Zhang X , KainzV , ZhaoJ , StrassmanAM , LevyD . Vascular extracellular signal-regulated kinase mediates migraine-related sensitization of meningeal nociceptors . Ann. Neurol.73 ( 6 ), 741 – 750 ( 2013 ).
  • Greco R , TassorelliC , ArmenteroMT , SandriniG , NappiG , BlandiniF . Role of central dopaminergic circuitry in pain processing and nitroglycerin-induced hyperalgesia . Brain Res.1238 , 215 – 223 ( 2008 ).
  • Bates EA , NikaiT , BrennanKCet al. Sumatriptan alleviates nitroglycerin-induced mechanical and thermal allodynia in mice . Cephalalgia30 ( 2 ), 170 – 178 ( 2010 ).
  • Ashina M , BendtsenL , JensenR , SakaiF , OlesenJ . Possible mechanisms of glyceryl-trinitrate-induced immediate headache in patients with chronic tension-type headache . Cephalalgia20 ( 10 ), 919 – 924 ( 2000 ).
  • Bigal ME , AshinaS , BursteinRet al. Prevalence and characteristics of allodynia in headache sufferers: a population study . Neurology70 ( 17 ), 1525 – 1533 ( 2008 ).
  • Sandkuhler J . Models and mechanisms of hyperalgesia and allodynia . Physiol. Rev.89 ( 2 ), 707 – 758 ( 2009 ).
  • Gazerani P , AndersenOK , Arendt-NielsenL . A human experimental capsaicin model for trigeminal sensitization. Gender-specific differences . Pain118 ( 1–2 ), 155 – 163 ( 2005 ).
  • Bittencourt Da Silva L , KarshenasA , BachFW , RasmussenS , Arendt-NielsenL , GazeraniP . Blockade of glutamate release by botulinum neurotoxin type A in humans: a dermal microdialysis study . Pain. Res. Manag.19 ( 3 ), 126 – 132 ( 2014 ).
  • Latremoliere A , WoolfCJ . Central sensitization: a generator of pain hypersensitivity by central neural plasticity . J. Pain10 ( 9 ), 895 – 926 ( 2009 ).
  • Simone DA , NolanoM , JohnsonT , Wendelschafer-CrabbG , KennedyWR . Intradermal injection of capsaicin in humans produces degeneration and subsequent reinnervation of epidermal nerve fibers: correlation with sensory function . J. Neurosci.18 ( 21 ), 8947 – 8954 ( 1998 ).
  • Schmelz M , PetersenLJ . Neurogenic inflammation in human and rodent skin . News Physiol. Sci.16 , 33 – 37 ( 2001 ).
  • Racine M , Tousignant-LaflammeY , KlodaLA , DionD , DupuisG , ChoiniereM . A systematic literature review of 10 years of research on sex/gender and experimental pain perception – Part 1: are there really differences between women and men?Pain153 ( 3 ), 602 – 618 ( 2012 ).
  • Racine M , Tousignant-LaflammeY , KlodaLA , DionD , DupuisG , ChoiniereM . A systematic literature review of 10 years of research on sex/gender and pain perception – Part 2: do biopsychosocial factors alter pain sensitivity differently in women and men?Pain153 ( 3 ), 619 – 635 ( 2012 ).
  • Macgregor EA , RosenbergJD , KurthT . Sex-related differences in epidemiological and clinic-based headache studies . Headache51 ( 6 ), 843 – 859 ( 2011 ).
  • Bolay H , BermanNEJ , AkcaliD . Sex-related differences in animal models of migraine headache . Headache51 ( 6 ), 891 – 904 ( 2011 ).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.