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Innervation extrakranialer Gewebe durch Kollateralen von Hirnhautafferenzen

Neue Einsichten in die Entstehung und Therapie von Kopfschmerzen

Innervation of extracranial tissues through collaterals of meningeal afferents

New insights into the generation and therapy of headaches

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Zusammenfassung

Die Dura mater encephali und große zerebrale Arterien gelten als die entscheidenden Strukturen, von denen Kopfschmerzen ausgehen, da ihre Reizung ausschließlich Kopfschmerzempfindungen hervorruft. Inwieweit auch extrakraniale Strukturen wie die Kopf- und Halsmuskulatur mit ihren Triggerpunkten daran beteiligt sind, wird immer wieder kritisch diskutiert. Als Erklärung für den Einfluss der extrakranialen nozizeptiven Vorgänge auf das Kopfschmerzgeschehen wird vor allem die konvergente afferente Innervation auf der Ebene der sekundären Neurone im trigemino-zervikalen Hirnstammkomplex genannt. Neue strukturelle und funktionelle Untersuchungen, insbesondere sogenannte Tracingexperimente bei Nagern und am Menschen, weisen aber deutlich darauf hin, dass Nervenfasern der Dura mater mit kollateralen Verzweigungen durch Suturen und Venenkanäle den Schädelknochen verlassen und Teile des äußeren Periost sowie tiefe Schichten der Kopfmuskulatur innervieren können. Bei noxischer Stimulation dieser extrakranialen Strukturen wird die Erregung auch in die meningealen Äste der afferenten Fasern fortgeleitet, wodurch Neuropeptide freigesetzt und die Hirnhautdurchblutung gesteigert werden können. Der Nachweis solcher extrakranialen Kollateralen meningealer Nervenfasern führt zu einer veränderten Sicht auf Vorgänge, die der Auslösung von Kopfschmerzen und ihrer therapeutischen Beeinflussung durch extrakraniale Manipulationen zu Grunde liegen.

Abstract

Headaches are believed to arise from the cranial dura mater and large cerebral arteries because stimuli applied to these structures cause exclusively headache-like sensations. The contribution of extracranial structures like head and neck muscles with their trigger points has also been discussed. The convergence of afferent input to the trigemino-cervical brainstem complex is mainly regarded as an explanation for the influence of extracranial nociceptive events on the headache generation. New structural and functional examinations, particularly tracing experiments in rodent and human tissues, show clearly that collaterals of meningeal nerve fibres penetrate the skull through sutures and along blood vessels to innervate parts of the outer periosteum and deep layers of pericranial muscles. Upon noxious stimulation of these extracranial structures the excitation spreads along these afferent branches into the meninges causing neuropeptide release and increased meningeal blood flow. The concept of an extracranial innervation by meningeal afferent collaterals offers a new explanation for the role of pericranial tissues in headache generation and the beneficial effects of therapeutic manipulations on these structures.

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Literatur

  1. Arnold F (1831) Der Kopfteil des vegetativen Nervensystems beim Menschen. Groos, Heidelberg

    Google Scholar 

  2. Luschka H (1856) Die Nerven der harten Hirnhaut. H. Laupp, Tübingen

    Google Scholar 

  3. Dowgjallo N (1929) Ueber die Nerven der harten Hirnhaut des Menschen and einiger Säuger. Z Anat Entwicklungsgesch 89:453–466

    Article  Google Scholar 

  4. Grzybowski J (1931) L’Innervation de la Dure – Mére cranienne chez l’homme. Arch Anat Histol Embryol 14:387–428

    Google Scholar 

  5. Ray BS, Wolff HG (1940) Experimental studies on headache: pain sensitive structures of the head and their significance in headache. Arch Surg 1:813–856

    Article  Google Scholar 

  6. Feindel W, Penfield W, McNaughton F (1960) The tentorial nerves and Iocalization of intracranial pain in man. Neurology 10:555–563

    Article  CAS  PubMed  Google Scholar 

  7. Penfield W, McNaughton M (1940) Dural headache and innervation of the dura mater. Arch Neurol Psychiatry 44:43–75

    Article  Google Scholar 

  8. Graham JR, Wolff HG (1938) Mechanism of migraine headache and action of ergotamine tartrate. Arch Neurol Psychiatry 39:737–763

    Article  CAS  Google Scholar 

  9. Bartsch T, Goadsby PJ (2011) Central mechanisms of peripheral nerve stimulation in headache disorders. Prog Neurol Surg 24:16–26. doi:10.1159/000323008

    Article  PubMed  Google Scholar 

  10. Olesen J, Burstein R, Ashina M, Tfelt-Hansen P (2009) Origin of pain in migraine: evidence for peripheral sensitisation. Lancet Neurol 8:679–690. doi:10.1016/S1474-4422(09)70090-0

    Article  PubMed  Google Scholar 

  11. Fernández-de-Las-Peñas C, Alonso-Blanco C, Cuadrado ML et al (2006) Myofascial trigger points and their relationship to headache clinical parameters in chronic tension-type headache. Headache 46:1264–1272. doi:10.1111/j.1526-4610.2006.00440.x

    Article  PubMed  Google Scholar 

  12. Fernández-de-las-Peñas C, Caminero AB, Madeleine P et al (2009) Multiple active myofascial trigger points and pressure pain sensitivity maps in the temporalis muscle are related in women with chronic tension type headache. Clin J Pain 25:506–512. doi:10.1097/AJP.0b013e3181a08747

    Article  PubMed  Google Scholar 

  13. Calandre EP, Hidalgo J, García-Leiva JM, Rico-Villademoros F (2006) Trigger point evaluation in migraine patients: an indication of peripheral sensitization linked to migraine predisposition? Eur J Neurol 13:244–249. doi:10.1111/j.1468-1331.2006.01181.x

    Article  CAS  PubMed  Google Scholar 

  14. Giamberardino MA, Tafuri E, Savini A et al (2007) Contribution of myofascial trigger points to migraine symptoms. J Pain 8:869–878. doi:10.1016/j.jpain.2007.06.002

    Article  PubMed  Google Scholar 

  15. Calandre EP, Hidalgo J, Garcia-Leiva JM et al (2008) Myofascial trigger points in cluster headache patients: a case series. Head Face Med 4:32. doi:10.1186/1746-160X-4-32

    Article  PubMed  PubMed Central  Google Scholar 

  16. Liu Y, Zhang M, Broman J, Edvinsson L (2003) Central projections of sensory innervation of the rat superficial temporal artery. Brain Res 966:126–133

    Article  CAS  PubMed  Google Scholar 

  17. Liu Y, Broman J, Edvinsson L (2004) Central projections of sensory innervation of the rat superior sagittal sinus. Neuroscience 129:431–437. doi:10.1016/j.neuroscience.2004.07.045

    Article  CAS  PubMed  Google Scholar 

  18. Burstein R, Yamamura H, Malick A, Strassman AM (1998) Chemical stimulation of the intracranial dura induces enhanced responses to facial stimulation in brain stem trigeminal neurons. J Neurophysiol 79:964–982

    CAS  PubMed  Google Scholar 

  19. Schepelmann K, Ebersberger A, Pawlak M et al (1999) Response properties of trigeminal brain stem neurons with input from dura mater encephali in the rat. Neuroscience 90:543–554

    Article  CAS  PubMed  Google Scholar 

  20. Malick A, Strassman RM, Burstein R (2000) Trigeminohypothalamic and reticulohypothalamic tract neurons in the upper cervical spinal cord and caudal medulla of the rat. J Neurophysiol 84:2078–2112

    CAS  PubMed  Google Scholar 

  21. Burstein R, Cutrer MF, Yarnitsky D (2000) The development of cutaneous allodynia during a migraine attack clinical evidence for the sequential recruitment of spinal and supraspinal nociceptive neurons in migraine. Brain J Neurol 123(Pt 8):1703–1709

    Article  Google Scholar 

  22. Goadsby PJ, Bartsch T, Dodick DW (2008) Occipital nerve stimulation for headache: mechanisms and efficacy. Headache 48:313–318. doi:10.1111/j.1526-4610.2007.01022.x

    Article  PubMed  Google Scholar 

  23. McMahon MS, Norregaard TV, Beyerl BD et al (1985) Trigeminal afferents to cerebral arteries and forehead are not divergent axon collaterals in cat. Neurosci Lett 60:63–68

    Article  CAS  PubMed  Google Scholar 

  24. O’Connor TP, van der Kooy D (1986) Pattern of intracranial and extracranial projections of trigeminal ganglion cells. J Neurosci 6:2200–2207

    PubMed  Google Scholar 

  25. Schaefer ML, Böttger B, Silver WL, Finger TE (2002) Trigeminal collaterals in the nasal epithelium and olfactory bulb: a potential route for direct modulation of olfactory information by trigeminal stimuli. J Comp Neurol 444:221–226. doi:10.1002/cne.10143

    Article  PubMed  Google Scholar 

  26. Kosaras B, Jakubowski M, Kainz V, Burstein R (2009) Sensory innervation of the calvarial bones of the mouse. J Comp Neurol 515:331–348. doi:10.1002/cne.22049

    PubMed  PubMed Central  Google Scholar 

  27. Schueler M, Neuhuber WL, De Col R, Messlinger K (2014) Innervation of rat and human dura mater and pericranial tissues in the parieto-temporal region by meningeal afferents. Headache 54:996–1009. doi:10.1111/head.12371

    Article  PubMed  Google Scholar 

  28. Messlinger K, Hanesch U, Baumgärtel M et al (1993) Innervation of the dura mater encephali of cat and rat: ultrastructure and calcitonin gene-related peptide-like and substance P‑like immunoreactivity. Anat Embryol (Berl) 188:219–237

    Article  CAS  Google Scholar 

  29. Messlinger K, Lennerz JK, Eberhardt M, Fischer MJM (2012) CGRP and NO in the trigeminal system: mechanisms and role in headache generation. Headache 52:1411–1427. doi:10.1111/j.1526-4610.2012.02212.x

    Article  PubMed  Google Scholar 

  30. Schueler M, Messlinger K, Dux M et al (2013) Extracranial projections of meningeal afferents and their impact on meningeal nociception and headache. Pain 154:1622–1631. doi:10.1016/j.pain.2013.04.040

    Article  PubMed  Google Scholar 

  31. Bruner E, Mantini S, Musso F et al (2011) The evolution of the meningeal vascular system in the human genus: From brain shape to thermoregulation. Am J Hum Biol 23:35–43. doi:10.1002/ajhb.21123

    Article  PubMed  Google Scholar 

  32. Holom VH, Messlinger K, Fischer MJM (2008) Temperature-dependent neuronal regulation of arterial blood flow in rat cranial dura mater. J Neurosci Res 86:158–164. doi:10.1002/jnr.21459

    Article  CAS  PubMed  Google Scholar 

  33. Reuter U, Bolay H, Jansen-Olesen I et al (2001) Delayed inflammation in rat meninges: implications for migraine pathophysiology. Brain 124:2490–2502

    Article  CAS  PubMed  Google Scholar 

  34. Strassman AM, Levy D (2006) Response properties of dural nociceptors in relation to headache. J Neurophysiol 95:1298–1306. doi:10.1152/jn.01293.2005

    Article  PubMed  Google Scholar 

  35. Strassman AM, Raymond SA, Burstein R (1996) Sensitization of meningeal sensory neurons and the origin of headaches. Nature 384:560–564. doi:10.1038/384560a0

    Article  CAS  PubMed  Google Scholar 

  36. Dux M, Sántha P, Jancsó G (2012) The role of chemosensitive afferent nerves and TRP ion channels in the pathomechanism of headaches. Pflugers Arch 464:239–248. doi:10.1007/s00424-012-1142-7

    Article  CAS  PubMed  Google Scholar 

  37. Wirth FP, Buren JM van (1971) Referral of pain from dural stimulation in man. J Neurosurg 34:630–642. doi:10.3171/jns.1971.34.5.0630

    Article  PubMed  Google Scholar 

  38. Franco AL, Gonçalves DAG, Castanharo SM et al (2010) Migraine is the most prevalent primary headache in individuals with temporomandibular disorders. J Orofac Pain 24:287–292

    PubMed  Google Scholar 

  39. Speciali JG, Dach F (2015) Temporomandibular dysfunction and headache disorder. Headache 55(Suppl 1):72–83. doi:10.1111/head.12515

    Article  PubMed  Google Scholar 

  40. Calhoun AH, Ford S, Millen C et al (2010) The prevalence of neck pain in migraine. Headache 50:1273–1277. doi:10.1111/j.1526-4610.2009.01608.x

    Article  PubMed  Google Scholar 

  41. Fernández-de-las-Peñas C, Ge H‑Y, Cuadrado ML et al (2008) Bilateral pressure pain sensitivity mapping of the temporalis muscle in chronic tension-type headache. Headache 48:1067–1075. doi:10.1111/j.1526-4610.2007.01005.x

    Article  PubMed  Google Scholar 

  42. Lozano López C, Mesa Jiménez J, de la Hoz Aizpurúa JL et al (2014) Efficacy of manual therapy in the treatment of tension-type headache. A systematic review from 2000–2013. Neurologia. doi:10.1016/j.nrl.2014.01.002

    PubMed  Google Scholar 

  43. Biondi DM (2005) Physical treatments for headache: a structured review. Headache 45:738–746. doi:10.1111/j.1526-4610.2005.05141.x

    Article  PubMed  Google Scholar 

  44. Fernández-de-Las-Peñas C, Cuadrado ML (2015) Physical therapy for headaches. Cephalalgia. doi:10.1177/0333102415596445

    Google Scholar 

  45. Schiapparelli P, Allais G, Rolando S et al (2011) Acupuncture in primary headache treatment. Neurol Sci 32(Suppl 1):15–18. doi:10.1007/s10072-011-0548-x

    Article  Google Scholar 

  46. Robbins MS, Kuruvilla D, Blumenfeld A et al (2014) Trigger point injections for headache disorders: expert consensus methodology and narrative review. Headache 54:1441–1459. doi:10.1111/head.12442

    Article  PubMed  Google Scholar 

  47. Ashkenazi A, Blumenfeld A (2013) OnabotulinumtoxinA for the treatment of headache. Headache 53(Suppl 2):54–61. doi:10.1111/head.12185

    Article  PubMed  Google Scholar 

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Danksagung

Die diesem Beitrag zu Grunde liegenden Projekte wurden durch die FAU Erlangen-Nürnberg (Emerging Fields Initiative), die Alexander von Humboldt-Stiftung (Reisestipendium für M. Dux) und die Europäische Union (FP7 Grant 602633 EUROHEADPAIN) unterstützt.

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Correspondence to K. Meßlinger.

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K. Meßlinger, M. Schüler, M. Dux, W.L. Neuhuber und R. De Col geben an, dass kein Interessenkonflikt besteht.

Die diesem Beitrag zu Grunde liegenden tierexperimentellen Untersuchungen wurden in Übereinstimmung mit den ethischen Richtlinien der International Association for the Study of Pain und der nationalen und europäischen Gesetzgebung (Council Directive 2010/63EU) durchgeführt und von der Bezirksregierung Mittelfranken genehmigt.

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Meßlinger, K., Schüler, M., Dux, M. et al. Innervation extrakranialer Gewebe durch Kollateralen von Hirnhautafferenzen. Manuelle Medizin 54, 307–314 (2016). https://doi.org/10.1007/s00337-016-0163-2

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