Skip to main content
Top
Published in: Current Pain and Headache Reports 9/2019

01-09-2019 | Central Nervous System Trauma | Secondary Headache (M Robbins, Section Editor)

Linking Traumatic Brain Injury, Sleep Disruption and Post-Traumatic Headache: a Potential Role for Glymphatic Pathway Dysfunction

Authors: Juan Piantino, Miranda M. Lim, Craig D. Newgard, Jeffrey Iliff

Published in: Current Pain and Headache Reports | Issue 9/2019

Login to get access

Abstract

Purpose of the Review

Traumatic brain injury (TBI) is a major public health concern in the USA and worldwide. Sleep disruption and headaches are two of the most common problems reported by patients after TBI. In this manuscript, we review the current knowledge regarding the relation between post-traumatic sleep disruption and headaches. We also describe the role of the glymphatic system as a potential link between TBI, sleep, and headaches.

Recent Findings

Recent studies show a reciprocal relation between post-traumatic sleep disruption and headaches: patients with sleep disruption after TBI report more headaches, and post-traumatic headaches are a risk factor for developing disrupted sleep. Despite this clinical association, the exact mechanisms linking post-traumatic sleep disruption and headaches are not well understood. The glymphatic pathway, a newly described brain–wide network of perivascular spaces that supports the clearance of interstitial solutes and wastes from the brain, is active primarily during sleep, and becomes dysfunctional after TBI. We propose a model where changes in glymphatic function caused by TBI and post-traumatic sleep disruption may impair the clearance of neuropeptides involved in the pathogenesis of post-traumatic headaches, such as CGRP.

Summary

The relation between TBI, post-traumatic sleep disruption, and post-traumatic headaches, although well documented in the literature, remains poorly understood. Dysfunction of the glymphatic system caused by TBI offers a novel and exiting explanation to this clinically observed phenomenon. The proposed model, although theoretical, could provide important mechanistic insights to the TBI-sleep-headache association.
Literature
1.
go back to reference Faul M XL, Wald MM, Coronado V. Traumatic brain injury in the United States. In: Centers for Disease Control and Prevention NCfIPaC, editor. Atlanta, GA2010. Faul M XL, Wald MM, Coronado V. Traumatic brain injury in the United States. In: Centers for Disease Control and Prevention NCfIPaC, editor. Atlanta, GA2010.
2.
go back to reference VA/DoD. Clinical practice guideline for management of concussion/mild traumatic brain injury. J Rehabil Res Dev. 2009;46(6):Cp1–68. VA/DoD. Clinical practice guideline for management of concussion/mild traumatic brain injury. J Rehabil Res Dev. 2009;46(6):Cp1–68.
3.
go back to reference Taylor CA, Bell JM, Breiding MJ, Xu L. Traumatic brain injury-related emergency department visits, hospitalizations, and deaths - United States, 2007 and 2013. Morbidity and mortality weekly report Surveillance summaries (Washington, DC : 2002). 2017;66(9):1–16. https://doi.org/10.15585/mmwr.ss6609a1.CrossRef Taylor CA, Bell JM, Breiding MJ, Xu L. Traumatic brain injury-related emergency department visits, hospitalizations, and deaths - United States, 2007 and 2013. Morbidity and mortality weekly report Surveillance summaries (Washington, DC : 2002). 2017;66(9):1–16. https://​doi.​org/​10.​15585/​mmwr.​ss6609a1.CrossRef
10.
go back to reference •• Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci Transl Med. 2012;4(147):147ra11. https://doi.org/10.1126/scitranslmed.3003748 First description of the role of the paravascular spaces in clearence of amyloid beta. CrossRef •• Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci Transl Med. 2012;4(147):147ra11. https://​doi.​org/​10.​1126/​scitranslmed.​3003748 First description of the role of the paravascular spaces in clearence of amyloid beta. CrossRef
11.
go back to reference •• Xie L, Kang H, Xu Q, Chen MJ, Liao Y, Thiyagarajan M et al First publication describing the increase in convective exchange of cerebrospinal fluid and interstitial fluid that occurs during sleep et al.. Science. 2013;342(6156):373–377. doi:https://doi.org/10.1126/science.1241224 Sleep drives metabolite clearance from the adult brain •• Xie L, Kang H, Xu Q, Chen MJ, Liao Y, Thiyagarajan M et al First publication describing the increase in convective exchange of cerebrospinal fluid and interstitial fluid that occurs during sleep et al.. Science. 2013;342(6156):373–377. doi:https://​doi.​org/​10.​1126/​science.​1241224 Sleep drives metabolite clearance from the adult brain
15.
go back to reference Watson NF, Dikmen S, Machamer J, Doherty M, Temkin N. Hypersomnia following traumatic brain injury. J Clin Sleep Med. 2007;3(4):363–8.PubMedPubMedCentral Watson NF, Dikmen S, Machamer J, Doherty M, Temkin N. Hypersomnia following traumatic brain injury. J Clin Sleep Med. 2007;3(4):363–8.PubMedPubMedCentral
16.
go back to reference • Wickwire EM, Williams SG, Roth T, Capaldi VF, Jaffe M, Moline M, et al. Sleep, sleep disorders, and mild traumatic brain injury. What we know and what we need to know: findings from a National Working Group. Neurotherapeutics. 2016;13(2):403–17. https://doi.org/10.1007/s13311-016-0429-3 A very good review on the current understanding of the relation between TBI and sleep disturbances. CrossRefPubMedPubMedCentral • Wickwire EM, Williams SG, Roth T, Capaldi VF, Jaffe M, Moline M, et al. Sleep, sleep disorders, and mild traumatic brain injury. What we know and what we need to know: findings from a National Working Group. Neurotherapeutics. 2016;13(2):403–17. https://​doi.​org/​10.​1007/​s13311-016-0429-3 A very good review on the current understanding of the relation between TBI and sleep disturbances. CrossRefPubMedPubMedCentral
17.
go back to reference Ouellet MC, Beaulieu-Bonneau S, Morin CM. Insomnia in patients with traumatic brain injury: frequency, characteristics, and risk factors. J Head Trauma Rehabil. 2006;21(3):199–212.CrossRef Ouellet MC, Beaulieu-Bonneau S, Morin CM. Insomnia in patients with traumatic brain injury: frequency, characteristics, and risk factors. J Head Trauma Rehabil. 2006;21(3):199–212.CrossRef
19.
go back to reference Clinchot DM, Bogner J, Mysiw WJ, Fugate L, Corrigan J. Defining sleep disturbance after brain injury. Am J Phys Med Rehabil. 1998;77(4):291–5.CrossRef Clinchot DM, Bogner J, Mysiw WJ, Fugate L, Corrigan J. Defining sleep disturbance after brain injury. Am J Phys Med Rehabil. 1998;77(4):291–5.CrossRef
21.
23.
go back to reference Castriotta RJ, Wilde MC, Lai JM, Atanasov S, Masel BE, Kuna ST. Prevalence and consequences of sleep disorders in traumatic brain injury. J Clin Sleep Med. 2007;3(4):349–56.PubMedPubMedCentral Castriotta RJ, Wilde MC, Lai JM, Atanasov S, Masel BE, Kuna ST. Prevalence and consequences of sleep disorders in traumatic brain injury. J Clin Sleep Med. 2007;3(4):349–56.PubMedPubMedCentral
38.
go back to reference Morin CM, Colecchi C, Stone J, Sood R, Brink D. Behavioral and pharmacological therapies for late-life insomnia: a randomized controlled trial. Jama. 1999;281(11):991–9.CrossRef Morin CM, Colecchi C, Stone J, Sood R, Brink D. Behavioral and pharmacological therapies for late-life insomnia: a randomized controlled trial. Jama. 1999;281(11):991–9.CrossRef
62.
81.
go back to reference Gawel MJ, Rothbart P, Jacobs H. Subcutaneous sumatriptan in the treatment of acute episodes of posttraumatic headache. Headache. 1993;33(2):96–7.CrossRef Gawel MJ, Rothbart P, Jacobs H. Subcutaneous sumatriptan in the treatment of acute episodes of posttraumatic headache. Headache. 1993;33(2):96–7.CrossRef
84.
go back to reference Abu-Arefeh I, Russell G. Prevalence of headache and migraine in schoolchildren. Bmj. 1994;309(6957):765–9.CrossRef Abu-Arefeh I, Russell G. Prevalence of headache and migraine in schoolchildren. Bmj. 1994;309(6957):765–9.CrossRef
90.
go back to reference Miller VA, Palermo TM, Powers SW, Scher MS, Hershey AD. Migraine headaches and sleep disturbances in children. Headache. 2003;43(4):362–8.CrossRef Miller VA, Palermo TM, Powers SW, Scher MS, Hershey AD. Migraine headaches and sleep disturbances in children. Headache. 2003;43(4):362–8.CrossRef
91.
go back to reference Barabas G, Ferrari M, Matthews WS. Childhood migraine and somnambulism. Neurology. 1983;33(7):948–9.CrossRef Barabas G, Ferrari M, Matthews WS. Childhood migraine and somnambulism. Neurology. 1983;33(7):948–9.CrossRef
92.
go back to reference Pradalier A, Giroud M, Dry J. Somnambulism, migraine and propranolol. Headache. 1987;27(3):143–5.CrossRef Pradalier A, Giroud M, Dry J. Somnambulism, migraine and propranolol. Headache. 1987;27(3):143–5.CrossRef
93.
go back to reference Dexter JD. The relationship between stage III + IV + REM sleep and arousals with migraine. Headache. 1979;19(7):364–9.CrossRef Dexter JD. The relationship between stage III + IV + REM sleep and arousals with migraine. Headache. 1979;19(7):364–9.CrossRef
101.
go back to reference Fialho LM, Pinho RS, Lin J, Minett TS, Vitalle MS, Fisberg M, et al. Sleep terrors antecedent is common in adolescents with migraine. Arq Neuropsiquiatr. 2013;71(2):83–6.CrossRef Fialho LM, Pinho RS, Lin J, Minett TS, Vitalle MS, Fisberg M, et al. Sleep terrors antecedent is common in adolescents with migraine. Arq Neuropsiquiatr. 2013;71(2):83–6.CrossRef
111.
go back to reference Kong J, Shepel PN, Holden CP, Mackiewicz M, Pack AI, Geiger JD. Brain glycogen decreases with increased periods of wakefulness: implications for homeostatic drive to sleep. J Neurosci. 2002;22(13):5581–7.CrossRef Kong J, Shepel PN, Holden CP, Mackiewicz M, Pack AI, Geiger JD. Brain glycogen decreases with increased periods of wakefulness: implications for homeostatic drive to sleep. J Neurosci. 2002;22(13):5581–7.CrossRef
115.
go back to reference Dodick DW, Eross EJ, Parish JM, Silber M. Clinical, anatomical, and physiologic relationship between sleep and headache. Headache. 2003;43(3):282–92.CrossRef Dodick DW, Eross EJ, Parish JM, Silber M. Clinical, anatomical, and physiologic relationship between sleep and headache. Headache. 2003;43(3):282–92.CrossRef
117.
go back to reference Zawilska JB, Skene DJ, Arendt J. Physiology and pharmacology of melatonin in relation to biological rhythms. Pharmacol Rep. 2009;61(3):383–410.CrossRef Zawilska JB, Skene DJ, Arendt J. Physiology and pharmacology of melatonin in relation to biological rhythms. Pharmacol Rep. 2009;61(3):383–410.CrossRef
138.
go back to reference Messlinger K, Hanesch U, Baumgartel M, Trost B, Schmidt RF. Innervation of the dura mater encephali of cat and rat: ultrastructure and calcitonin gene-related peptide-like and substance P-like immunoreactivity. Anat Embryol. 1993;188(3):219–37.CrossRef Messlinger K, Hanesch U, Baumgartel M, Trost B, Schmidt RF. Innervation of the dura mater encephali of cat and rat: ultrastructure and calcitonin gene-related peptide-like and substance P-like immunoreactivity. Anat Embryol. 1993;188(3):219–37.CrossRef
141.
go back to reference Lennerz JK, Ruhle V, Ceppa EP, Neuhuber WL, Bunnett NW, Grady EF, et al. Calcitonin receptor-like receptor (CLR), receptor activity-modifying protein 1 (RAMP1), and calcitonin gene-related peptide (CGRP) immunoreactivity in the rat trigeminovascular system: differences between peripheral and central CGRP receptor distribution. J Comp Neurol. 2008;507(3):1277–99. https://doi.org/10.1002/cne.21607.CrossRefPubMed Lennerz JK, Ruhle V, Ceppa EP, Neuhuber WL, Bunnett NW, Grady EF, et al. Calcitonin receptor-like receptor (CLR), receptor activity-modifying protein 1 (RAMP1), and calcitonin gene-related peptide (CGRP) immunoreactivity in the rat trigeminovascular system: differences between peripheral and central CGRP receptor distribution. J Comp Neurol. 2008;507(3):1277–99. https://​doi.​org/​10.​1002/​cne.​21607.CrossRefPubMed
Metadata
Title
Linking Traumatic Brain Injury, Sleep Disruption and Post-Traumatic Headache: a Potential Role for Glymphatic Pathway Dysfunction
Authors
Juan Piantino
Miranda M. Lim
Craig D. Newgard
Jeffrey Iliff
Publication date
01-09-2019
Publisher
Springer US
Published in
Current Pain and Headache Reports / Issue 9/2019
Print ISSN: 1531-3433
Electronic ISSN: 1534-3081
DOI
https://doi.org/10.1007/s11916-019-0799-4

Other articles of this Issue 9/2019

Current Pain and Headache Reports 9/2019 Go to the issue

Secondary Headache (M Robbins, Section Editor)

Migraine as a Stroke Mimic and as a Stroke Chameleon

Uncommon and/or Unusual Headaches and Syndromes (J Ailani, Section Editor)

Presentation and Management of Headache in Pituitary Apoplexy

Hot Topics in Pain and Headache (N Rosen, Section Editor)

Treatment Strategies and Effective Management of Phantom Limb–Associated Pain