Sono pobre e diminuição da espessura cortical em veteranos com lesão cerebral traumática leve e transtorno de estresse pós-traumático

  • role: First author第一作者
  • Affiliation:

    Boston University Chobanian and Avedisian School of Medicine, Boston, MA 02118, USA

    Translational Research Center for TBI and Stress Disorders (TRACTS), VA Boston Healthcare System, Boston, MA 02130, USA

Murray J. Andrews12,  
  • Affiliation:

    Department of Psychiatry, Harvard Medical School, Boston, MA 02138, USA

    Department f Psychiatry, Boston University School of Medicine, Boston, MA 02130, USA

    Neuroimaging Research for Veterans Center, VA Boston Healthcare System, Boston, MA 02130, USA

    Anthinoula A. Martinos Center for Biomedical Imaging, Boston, MA 02129, USA

David H. Salat3456,  
  • Affiliation:

    Translational Research Center for TBI and Stress Disorders (TRACTS), VA Boston Healthcare System, Boston, MA 02130, USA

    Department of Psychiatry, Harvard Medical School, Boston, MA 02138, USA

    Geriatric Research, Educational and Clinical Center (GRECC), VA Boston Healthcare System, Boston, MA 02130, USA

William P. Milberg237,  
  • Affiliation:

    Translational Research Center for TBI and Stress Disorders (TRACTS), VA Boston Healthcare System, Boston, MA 02130, USA

    Department of Psychiatry, Harvard Medical School, Boston, MA 02138, USA

    Geriatric Research, Educational and Clinical Center (GRECC), VA Boston Healthcare System, Boston, MA 02130, USA

Regina E. McGlinchey237,  
  • role: Corresponding author通信作者
  • Affiliation:

    Translational Research Center for TBI and Stress Disorders (TRACTS), VA Boston Healthcare System, Boston, MA 02130, USA

    Department of Psychiatry, Harvard Medical School, Boston, MA 02138, USA

    Geriatric Research, Educational and Clinical Center (GRECC), VA Boston Healthcare System, Boston, MA 02130, USA

  • Email:catherine_fortier@hms.harvard.edu
  • Introduction:* catherine_fortier@hms.harvard.edu
Catherine B. Fortier237*

Resumo

Background:Poor sleep quality has been associated with changes in brain volume among veterans, particularly those who have experienced mild traumatic brain injury (mTBI) and post-traumatic stress disorder (PTSD). This study sought to investigate: 1) whether poor sleep quality is associated with decreased cortical thickness in Iraq and Afghanistan war veterans, and 2) whether these associations differ topographically depending on the presence or absence of mTBI and PTSD.Methods:A sample of 440 post-9/11 era U.S. veterans enrolled in the Translational Research Center for Traumatic Brain Injury and Stress Disorders study at VA Boston, MA from 2010 to 2022 was included in the study. We examined the relationship between sleep quality, as measured by the Pittsburgh Sleep Quality Index (PSQI), and cortical thickness in veterans with mTBI (n=57), PTSD (n=110), comorbid mTBI and PTSD (n=129), and neither PTSD nor mTBI (n=144). To determine the topographical relationship between subjective sleep quality and cortical thickness in each diagnostic group, we employed a General Linear Model (GLM) at each vertex on the cortical mantle. The extent of topographical overlap between the resulting statistical maps was assessed using Dice coefficients.Results:There were no significant associations between PSQI and cortical thickness in the group without PTSD or mTBI (n=144) or in the PTSD-only group (n=110). In the mTBI-only group (n=57), lower sleep quality was significantly associated with reduced thickness bilaterally in frontal, cingulate, and precuneus regions, as well as in the right parietal and temporal regions (β=–0.0137, P<0.0005). In the comorbid mTBI and PTSD group (n=129), significant associations were observed bilaterally in frontal, precentral, and precuneus regions, in the left cingulate and the right parietal regions (β=–0.0094, P<0.0005). Interaction analysis revealed that there was a stronger relationship between poor sleep quality and decreased cortical thickness in individuals with mTBI (n=186) compared with those without mTBI (n=254) specifically in the frontal and cingulate regions (β=–0.0077, P<0.0005).Conclusions:This study demonstrates a significant relationship between poor sleep quality and lower cortical thickness primarily within frontal regions among individuals with both isolated mTBI or comorbid diagnoses of mTBI and PTSD. Thus, if directionality is established in longitudinal and interventional studies, it may be crucial to consider addressing sleep in the treatment of veterans who have sustained mTBI.

Palavras-chave

Trauma;Brain injury;Sleep;Veterans;Cortical thickness

References

  1. 1..
    Capaldi VF II, Guerrero ML, Killgore WDS. Sleep disruptions among returning combat veterans from Iraq and Afghanistan. Mil Med. 2011;176(8):879–88.
  2. 2..
    Lewis V, Creamer M, Failla S. Is poor sleep in veterans a function of posttraumatic stress disorder?. Mil Med. 2009;174(9):948–51.
  3. 3..
    Videnovic A, Lazar AS, Barker RA, Overeem S. ’The clocks that time us’-circadian rhythms in neurodegenerative disorders. Nat Rev Neurol. 2014;10(12):683–93.
  4. 4..
    Bubu OM, Brannick M, Mortimer J, Umasabor-Bubu O, Sebastião YV, Wen Y, et al. Sleep, cognitive impairment, and Alzheimer’s disease: a systematic review and meta-analysis. Sleep. 2017. .
  5. 5..
    Fjell AM, Sørensen Ø, Amlien IK, Bartrés-Faz D, Brandmaier AM, Buchmann N, et al. Poor self-reported sleep is related to regional cortical thinning in aging but not memory decline-results from the lifebrain consortium. Cereb Cortex. 2021;31(4):1953–69.
  6. 6..
    Stoffers D, Moens S, Benjamins J, van Tol MJ, Penninx BWJH, Veltman DJ, et al. Orbitofrontal gray matter relates to early morning awakening: a neural correlate of insomnia complaints?. Front Neurol. 2012;3:105.
  7. 7..
    Reinhard MA, Regen W, Baglioni C, Nissen C, Feige B, Hennig J, et al. The relationship between brain morphology and polysomnography in healthy good sleepers. PLoS One. 2014;9(10):e109336.
  8. 8..
    Lim ASP, Fleischman DA, Dawe RJ, Yu L, Arfanakis K, Buchman AS, et al. Regional neocortical gray matter structure and sleep fragmentation in older adults. Sleep. 2016;39(1):227–35.
  9. 9..
    Grau-Rivera O, Operto G, Falcón C, Sánchez-Benavides G, Cacciaglia R, Brugulat-Serrat A, et al. Association between insomnia and cognitive performance, gray matter volume, and white matter microstructure in cognitively unimpaired adults. Alzheimers Res Ther. 2020;12(1):4.
  10. 10..
    Carvalho DZ, St Louis EK, Boeve BF, Mielke MM, Przybelski SA, Knopman DS, et al. Excessive daytime sleepiness and fatigue may indicate accelerated brain aging in cognitively normal late middle-aged and older adults. Sleep Med. 2017;32:236–43.
  11. 11..
    Del Brutto OH, Mera RM, Zambrano M, Castillo PR. The association between poor sleep quality and global cortical atrophy is related to age. Results from the Atahualpa Project. Sleep Sci Sao Paulo Braz. 2016;9(3):147–50.
  12. 12..
    Branger P, Arenaza-Urquijo EM, Tomadesso C, Mézenge F, André C, de Flores R, et al. Relationships between sleep quality and brain volume, metabolism, and amyloid deposition in late adulthood. Neurobiol Aging. 2016;41:107–14.
  13. 13..
    Alperin N, Wiltshire J, Lee SH, Ramos AR, Hernandez-Cardenache R, Rundek T, et al. Effect of sleep quality on amnestic mild cognitive impairment vulnerable brain regions in cognitively normal elderly individuals. Sleep. 2019;42(3):zsy254.
  14. 14..
    Stolicyn A, Lyall LM, Lyall DM, Høier NK, Adams MJ, Shen X, et al. Comprehensive assessment of sleep duration, insomnia, and brain structure within the UK Biobank cohort. Sleep. 2024;47(2):zsad274.
  15. 15..
    Tsiknia AA, JrParada H, Banks SJ, Reas ET. Sleep quality and sleep duration predict brain microstructure among community-dwelling older adults. Neurobiol Aging. 2023;125:90–7.
  16. 16..
    Li Y, Wang J, Ji L, Cheng C, Su T, Wu S, et al. Cortical thinning in male obstructive sleep apnoea patients with excessive daytime sleepiness. Front Neurol. 2023;14:1019457.
  17. 17..
    Hoge CW, Castro CA, Messer SC, McGurk D, Cotting DI, Koffman RL. Combat duty in Iraq and Afghanistan, mental health problems, and barriers to care. N Engl J Med. 2004;351(1):13–22.
  18. 18..
    Hoge CW, McGurk D, Thomas JL, Cox AL, Engel CC, Castro CA. Mild traumatic brain injury in U.S. Soldiers returning from Iraq. N Engl J Med. 2008;358(5):453–63.
  19. 19..
    Lindquist LK, Love HC, Elbogen EB. Traumatic brain injury in Iraq and Afghanistan veterans: new results from a national random sample study. J Neuropsychiatry Clin Neurosci. 2017;29(3):254–9.
  20. 20..
    Nardo D, Högberg G, Looi JCL, Larsson S, Hällström T, Pagani M. Gray matter density in limbic and paralimbic cortices is associated with trauma load and EMDR outcome in PTSD patients. J Psychiatr Res. 2010;44(7):477–85.
  21. 21..
    Herringa R, Phillips M, Almeida J, Insana S, Germain A. Post-traumatic stress symptoms correlate with smaller subgenual cingulate, caudate, and insula volumes in unmedicated combat veterans. Psychiatry Res. 2012;203(2–3):139–45.
  22. 22..
    Lindemer ER, Salat DH, Leritz EC, McGlinchey RE, Milberg WP. Reduced cortical thickness with increased lifetime burden of PTSD in OEF/OIF Veterans and the impact of comorbid TBI. Neuroimage Clin. 2013;2:601–11.
  23. 23..
    Govindarajan KA, Narayana PA, Hasan KM, Wilde EA, Levin HS, Hunter JV, et al. Cortical thickness in mild traumatic brain injury. J Neurotrauma. 2016;33(20):1809–17.
  24. 24..
    Michael AP, Stout J, Roskos PT, Bolzenius J, Gfeller J, Mogul D, et al. Evaluation of cortical thickness after traumatic brain injury in military veterans. J Neurotrauma. 2015;32(22):1751–8.
  25. 25..
    Tate DF, York GE, Reid MW, Cooper DB, Jones L, Robin DA, et al. Preliminary findings of cortical thickness abnormalities in blast injured service members and their relationship to clinical findings. Brain Imaging Behav. 2014;8(1):102–9.
  26. 26..
    Seo J, Oliver KI, Daffre C, Pace-Schott EF. 0867 relationships of sleep with cortical thickness in trauma exposed individuals with and without PTSD. Sleep. 2019;42(Suppl 1):A348–9.
  27. 27..
    Dailey NS, Raikes AC, Alkozei A, Grandner MA, Killgore WD. 0014 reduced cortical thickness as a biomarker of daytime sleepiness in mild traumatic brain injury. Sleep. 2020;43(Suppl 1):A5-6.
  28. 28..
    Nardo D, Högberg G, Jonsson C, Jacobsson H, Hällström T, Pagani M. Neurobiology of sleep disturbances in PTSD patients and traumatized controls: MRI and SPECT findings. Front Psychiatry. 2015;6:134.
  29. 29..
    Chao LL, Mohlenhoff BS, Weiner MW, Neylan TC. Associations between subjective sleep quality and brain volume in Gulf War veterans. Sleep. 2014;37(3):445–52.
  30. 30..
    Fortier CB, Amick MM, Grande L, McGlynn S, Kenna A, Morra L, et al. The Boston assessment of traumatic brain injury-lifetime (BAT-L) semistructured interview: evidence of research utility and validity. J Head Trauma Rehabil. 2014;29(1):89–98.
  31. 31..
    Yurgil KA, Barkauskas DA, Vasterling JJ, Nievergelt CM, Larson GE, Schork NJ, et al. Association between traumatic brain injury and risk of posttraumatic stress disorder in active-duty Marines. JAMA Psychiat. 2014;71(2):149–57.
  32. 32..
    Spira AP, Gonzalez CE, Venkatraman VK, Wu MN, Pacheco J, Simonsick EM, et al. Sleep duration and subsequent cortical thinning in cognitively normal older adults. Sleep. 2016;39(5):1121–8.
  33. 33..
    McGlinchey RE, Milberg WP, Fonda JR, Fortier CB. A methodology for assessing deployment trauma and its consequences in OEF/OIF/OND veterans: the TRACTS longitudinal prospective cohort study. Int J Methods Psychiatr Res. 2017;26(3):e1556.
  34. 34..
    Blake DD, Weathers FW, Nagy LM, Kaloupek DG, Gusman FD, Charney DS, et al. The development of a Clinician-Administered PTSD Scale. J Trauma Stress. 1995;8(1):75–90.
  35. 35..
    Jackson CE, Currao A, Fonda JR, Kenna A, Milberg WP, McGlinchey RE, et al. Research utility of a CAPS-IV and CAPS-5 hybrid interview: posttraumatic stress symptom and diagnostic concordance in recent-era U.S. veterans. J Trauma Stress. 2022;35(2):570–80.
  36. 36..
    Lovibond SH, Lovibond PF. Manual for the depression anxiety stress scales. Syd Psychol Found Aust. 1995. .
  37. 37..
    Lovibond PF, Lovibond SH. The structure of negative emotional states: comparison of the Depression Anxiety Stress Scales (DASS) with the Beck Depression and Anxiety Inventories. Behav Res Ther. 1995;33(3):335–43.
  38. 38..
    Buysse DJ, 3rdReynolds CF, Monk TH, Berman SR, Kupfer DJ. The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989;28(2):193–213.
  39. 39..
    Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis. I. segmentation and surface reconstruction. Neuroimage. 1999;9(2):179–94.
  40. 40..
    Fischl B, Sereno MI, Dale AM. Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage. 1999;9(2):195–207.
  41. 41..
    Fischl B, Dale AM. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci U S A. 2000;97(20):11050–5.
  42. 42..
    Dice LR. Measures of the amount of ecologic association between species. Ecology. 1945;26(3):297–302.
  43. 43..
    Bigler ED. Anterior and middle cranial fossa in traumatic brain injury: relevant neuroanatomy and neuropathology in the study of neuropsychological outcome. Neuropsychology. 2007;21(5):515–31.
  44. 44..
    Bremner JD, Randall P, Scott TM, Bronen RA, Seibyl JP, Southwick SM, et al. MRI-based measurement of hippocampal volume in patients with combat-related posttraumatic stress disorder. Am J Psychiatry. 1995;152(7):973–81.
  45. 45..
    Karl A, Schaefer M, Malta LS, Dörfel D, Rohleder N, Werner A. A meta-analysis of structural brain abnormalities in PTSD. Neurosci Biobehav Rev. 2006;30(7):1004–31.
  46. 46..
    Rojczyk P, Seitz-Holland J, Kaufmann E, Sydnor VJ, Kim CL, Umminger LF, et al. Sleep quality disturbances are associated with white matter alterations in veterans with post-traumatic stress disorder and mild traumatic brain injury. J Clin Med. 2023;12(5):2079.
  47. 47..
    Gupte R, Brooks W, Vukas R, Pierce J, Harris J. Sex differences in traumatic brain injury: what we know and what we should know. J Neurotrauma. 2019;36(22):3063–91.
  48. 48..
    Roeckner AR, Sogani S, Michopoulos V, Hinrichs R, van Rooij SJH, Rothbaum BO, et al. Sex-dependent risk factors for PTSD: a prospective structural MRI study. Neuropsychopharmacology. 2022;47(13):2213–20.
  49. 49..
    Ioannides AA, Kostopoulos GK, Liu L, Fenwick PBC. MEG identifies dorsal medial brain activations during sleep. Neuroimage. 2009;44(2):455–68.
  50. 50..
    Murphy M, Riedner BA, Huber R, Massimini M, Ferrarelli F, Tononi G. Source modeling sleep slow waves. Proc Natl Acad Sci U S A. 2009;106(5):1608–13.
  51. 51..
    Koenigs M, Holliday J, Solomon J, Grafman J. Left dorsomedial frontal brain damage is associated with insomnia. J Neurosci. 2010;30(47):16041–3.
  52. 52..
    Morawska MM, Büchele F, Moreira CG, Imbach LL, Noain D, Baumann CR. Sleep modulation alleviates axonal damage and cognitive decline after rodent traumatic brain injury. J Neurosci Off J Soc Neurosci. 2016;36(12):3422–9.
  53. 53..
    Baumann CR, Werth E, Stocker R, Ludwig S, Bassetti CL. Sleep-wake disturbances 6 months after traumatic brain injury: a prospective study. Brain. 2007;130(Pt 7):1873–83.
  54. 54..
    Aoun R, Rawal H, Attarian H, Sahni A. Impact of traumatic brain injury on sleep: an overview. Nat Sci Sleep. 2019;11:131–40.
  55. 55..
    Gardani M, Morfiri E, Thomson A, O’Neill B, McMillan TM. Evaluation of sleep disorders in patients with severe traumatic brain injury during rehabilitation. Arch Phys Med Rehabil. 2015;96(9):1691-1697.e3.
  56. 56..
    Brown EM, Salat DH, Milberg WP, Fortier CB, McGlinchey RE. Accelerated longitudinal cortical atrophy in OEF/OIF/OND veterans with severe PTSD and the impact of comorbid TBI. Hum Brain Mapp. 2022;43(12):3694–705.

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