Dynamic changes in perivascular space morphology predict signs of spaceflight-associated neuro-ocular syndrome in bed rest.
Journal
NPJ microgravity
ISSN: 2373-8065
Titre abrégé: NPJ Microgravity
Pays: United States
ID NLM: 101703605
Informations de publication
Date de publication:
01 Mar 2024
01 Mar 2024
Historique:
received:
03
08
2023
accepted:
15
02
2024
medline:
2
3
2024
pubmed:
2
3
2024
entrez:
1
3
2024
Statut:
epublish
Résumé
During long-duration spaceflight, astronauts experience headward fluid shifts and expansion of the cerebral perivascular spaces (PVS). A major limitation to our understanding of the changes in brain structure and physiology induced by spaceflight stems from the logistical difficulties of studying astronauts. The current study aimed to determine whether PVS changes also occur on Earth with the spaceflight analog head-down tilt bed rest (HDBR). We examined how the number and morphology of magnetic resonance imaging-visible PVS (MV-PVS) are affected by HDBR with and without elevated carbon dioxide (CO
Identifiants
pubmed: 38429289
doi: 10.1038/s41526-024-00368-6
pii: 10.1038/s41526-024-00368-6
doi:
Types de publication
Journal Article
Langues
eng
Pagination
24Subventions
Organisme : National Aeronautics and Space Administration (NASA)
ID : 80NSSC17K0021
Organisme : National Aeronautics and Space Administration (NASA)
ID : 80NSSC18K0783
Informations de copyright
© 2024. The Author(s).
Références
Iliff, J. J. et al. Brain-wide pathway for waste clearance captured by contrast-enhanced MRI. J. Clin. Invest. 123, 1299–1309 (2013).
pubmed: 23434588
pmcid: 3582150
doi: 10.1172/JCI67677
Iliff, J. J. et al. A Paravascular Pathway Facilitates CSF Flow Through the Brain Parenchyma and the Clearance of Interstitial Solutes, Including Amyloid Beta. Sci. Transl. Med. 4, 1–22 (2012).
doi: 10.1126/scitranslmed.3003748
Bacyinski, A., Xu, M., Wang, W. & Hu, J. The Paravascular Pathway for Brain Waste Clearance: Current Understanding, Significance and Controversy. Front Neuroanat. 11, 101 (2017).
pubmed: 29163074
pmcid: 5681909
doi: 10.3389/fnana.2017.00101
Troili, F. et al. Perivascular Unit: This Must Be the Place. The Anatomical Crossroad Between the Immune, Vascular and Nervous System. Front Neuroanat. 14, 17 (2020).
pubmed: 32372921
pmcid: 7177187
doi: 10.3389/fnana.2020.00017
Nedergaard, M. & Goldman, S. A. Brain Drain. Sci. Am. 314, 44–49 (2016).
pubmed: 27066643
pmcid: 5347443
doi: 10.1038/scientificamerican0316-44
Ramirez, J. et al. Visible Virchow-Robin spaces on magnetic resonance imaging of Alzheimer’s disease patients and normal elderly from the Sunnybrook Dementia Study. J. Alzheimers Dis. 43, 415–424 (2015).
pubmed: 25096616
doi: 10.3233/JAD-132528
Potter, G. M., Chappell, F. M., Morris, Z. & Wardlaw, J. M. Cerebral perivascular spaces visible on magnetic resonance imaging: development of a qualitative rating scale and its observer reliability. Cerebrovasc. Dis. 39, 224–231 (2015).
pubmed: 25823458
pmcid: 4386144
doi: 10.1159/000375153
Charidimou, A. et al. White matter perivascular spaces: An MRI marker in pathology-proven cerebral amyloid angiopathy? Neurology 82, 57–62 (2014).
pubmed: 24285616
pmcid: 3873625
doi: 10.1212/01.wnl.0000438225.02729.04
Inglese, M. et al. Clinical significance of dilated Virchow-Robin spaces in mild traumatic brain injury. Brain Inj. 20, 15–21 (2006).
pubmed: 16403696
doi: 10.1080/02699050500309593
Patankar, T. F. et al. Dilatation of the Virchow-Robin Space Is a Sensitive Indicator of Cerebral Microvascular Disease: Study in Elderly Patients with Dementia. AJNR Am. J. Neuroradiol. 26, 1512–1520 (2005).
pubmed: 15956523
pmcid: 8149063
Opel, R. A. et al. Effects of traumatic brain injury on sleep and enlarged perivascular spaces. J. Cereb. Blood Flow. Metab. 39, 2258–2267 (2019).
pubmed: 30092696
doi: 10.1177/0271678X18791632
Hupfeld, K. E. et al. Longitudinal MRI-visible perivascular space (PVS) changes with long-duration spaceflight. Sci. Rep. 12, 7238 (2022).
pubmed: 35513698
pmcid: 9072425
doi: 10.1038/s41598-022-11593-y
Barisano, G. et al. The effect of prolonged spaceflight on cerebrospinal fluid and perivascular spaces of astronauts and cosmonauts. Proc. Natl. Acad. Sci. USA 119, e2120439119 (2022).
pubmed: 35412862
pmcid: 9169932
doi: 10.1073/pnas.2120439119
Koppelmans, V., Bloomberg, J. J., Mulavara, A. P. & Seidler, R. D. Brain structural plasticity with spaceflight. NPJ Microgravity 2, 1–8 (2016).
doi: 10.1038/s41526-016-0001-9
Roberts, D. R. et al. Effects of Spaceflight on Astronaut Brain Structure as Indicated on MRI. N. Engl. J. Med. 377, 1746–1753 (2017).
pubmed: 29091569
doi: 10.1056/NEJMoa1705129
Lee, J. K. et al. Spaceflight-Associated Brain White Matter Microstructural Changes and Intracranial Fluid Redistribution. JAMA Neurol. 76, 412–419 (2019).
pubmed: 30673793
pmcid: 6459132
doi: 10.1001/jamaneurol.2018.4882
Hargens, A. R. & Vico, L. Long-duration bed rest as an analog to microgravity. J. Appl Physiol. 120, 891–903 (2016).
pubmed: 26893033
doi: 10.1152/japplphysiol.00935.2015
Mulavara, A. P. et al. Physiological and Functional Alterations after Spaceflight and Bed Rest. Med Sci. Sports Exerc. 50, 1961–1980 (2018).
pubmed: 29620686
pmcid: 6133205
doi: 10.1249/MSS.0000000000001615
Law, J. et al. Relationship between carbon dioxide levels and reported headaches on the international space station. J. Occup. Environ. Med 56, 477–483 (2014).
pubmed: 24806559
doi: 10.1097/JOM.0000000000000158
Battisti-Charbonney, A., Fisher, J. & Duffin, J. The cerebrovascular response to carbon dioxide in humans. J. Physiol. 589, 3039–3048 (2011).
pubmed: 21521758
pmcid: 3139085
doi: 10.1113/jphysiol.2011.206052
Zong, X. et al. Morphology of perivascular spaces and enclosed blood vessels in young to middle-aged healthy adults at 7T: Dependences on age, brain region, and breathing gas. Neuroimage 218, 116978 (2020).
pubmed: 32447015
doi: 10.1016/j.neuroimage.2020.116978
Laurie, S. S. et al. Optic Disc Edema after 30 Days of Strict Head-down Tilt Bed Rest. Ophthalmology 126, 467–468 (2019).
pubmed: 30308219
doi: 10.1016/j.ophtha.2018.09.042
Yang, J. W. et al. Spaceflight-associated neuro-ocular syndrome: a review of potential pathogenesis and intervention. Int J. Ophthalmol. 15, 336–341 (2022).
pubmed: 35186696
pmcid: 8818462
doi: 10.18240/ijo.2022.02.21
Lee, A. G. et al. Spaceflight associated neuro-ocular syndrome (SANS) and the neuro-ophthalmologic effects of microgravity: a review and an update. NPJ Microgravity 6, 1–7 (2020).
Wostyn, P., Killer, H. E. & De Deyn, P. P. Why a One-Way Ticket to Mars May Result in a One-Way Directional Glymphatic Flow to the Eye. J. Neuro-Ophthalmol. 37, 462–463 (2017).
doi: 10.1097/WNO.0000000000000578
Mader, T. H. et al. Persistent Globe Flattening in Astronauts following Long-Duration Spaceflight. Neuroophthalmology 45, 29–35 (2021).
pubmed: 33762785
doi: 10.1080/01658107.2020.1791189
Wostyn, P., Gibson, C. R. & Mader, T. H. The odyssey of the ocular and cerebrospinal fluids during a mission to Mars: the “ocular glymphatic system” under pressure. Eye (Lond.) 36, 686–691 (2022).
pubmed: 34373611
doi: 10.1038/s41433-021-01721-9
Wostyn, P., Mader, T. H., Gibson, C. R. & Nedergaard, M. Does Long-Duration Exposure to Microgravity Lead to Dysregulation of the Brain and Ocular Glymphatic Systems? Eye Brain 14, 49–58 (2022).
pubmed: 35546965
pmcid: 9081191
doi: 10.2147/EB.S354710
Zwart, S. R. et al. Association of Genetics and B Vitamin Status With the Magnitude of Optic Disc Edema During 30-Day Strict Head-Down Tilt Bed Rest. JAMA Ophthalmol. 137, 1195–1200 (2019).
pubmed: 31415055
pmcid: 6696878
doi: 10.1001/jamaophthalmol.2019.3124
Zwart, S. R. et al. Vision changes after spaceflight are related to alterations in folate- and vitamin B-12-dependent one-carbon metabolism. J. Nutr. 142, 427–431 (2012).
pubmed: 22298570
doi: 10.3945/jn.111.154245
Smith, S. M. & Zwart, S. R. Spaceflight-related ocular changes: the potential role of genetics, and the potential of B vitamins as a countermeasure. Curr. Opin. Clin. Nutr. Metab. Care 21, 481–488 (2018).
pubmed: 30169456
doi: 10.1097/MCO.0000000000000510
Clement, G. et al. Assessing the effects of artificial gravity in an analog of long-duration spaceflight: The protocol and implementation of the AGBRESA bed rest study. Front Physiol. 13, 976926 (2022).
pubmed: 36160844
pmcid: 9492851
doi: 10.3389/fphys.2022.976926
Clément, G. R. et al. International standard measures during the AGBRESA bed rest study. Acta Astronautica 200, 163–175 (2022).
doi: 10.1016/j.actaastro.2022.08.016
Tays, G. D. et al. The Effects of 30 min of Artificial Gravity on Cognitive and Sensorimotor Performance in a Spaceflight Analog Environment. Front. Neural. Circuits 16, 784280 (2022).
pubmed: 35310547
pmcid: 8924040
doi: 10.3389/fncir.2022.784280
Taoka, T. et al. Evaluation of glymphatic system activity with the diffusion MR technique: diffusion tensor image analysis along the perivascular space (DTI-ALPS) in Alzheimer’s disease cases. Jpn J. Radio. 35, 172–178 (2017).
doi: 10.1007/s11604-017-0617-z
Liu, H. et al. Associations Among Diffusion Tensor Image Along the Perivascular Space (DTI-ALPS), Enlarged Perivascular Space (ePVS), and Cognitive Functions in Asymptomatic Patients With Carotid Plaque. Front Neurol. 12, 789918 (2021).
pubmed: 35082748
doi: 10.3389/fneur.2021.789918
Taoka, T. et al. Reproducibility of diffusion tensor image analysis along the perivascular space (DTI-ALPS) for evaluating interstitial fluid diffusivity and glymphatic function: CHanges in Alps index on Multiple conditiON acquIsition eXperiment (CHAMONIX) study. Jpn J. Radio. 40, 147–158 (2022).
doi: 10.1007/s11604-021-01187-5
Lee, J. K. et al. Effects of Spaceflight Stressors on Brain Volume, Microstructure, and Intracranial Fluid Distribution. Cereb. Cortex Commun. 2, 1–14 (2021).
Lee, J. K. et al. Head Down Tilt Bed Rest Plus Elevated CO2 as a Spaceflight Analog: Effects on Cognitive and Sensorimotor Performance. Front Hum. Neurosci. 13, 355 (2019).
pubmed: 31680909
pmcid: 6811492
doi: 10.3389/fnhum.2019.00355
Berezuk, C. et al. Virchow-Robin Spaces: Correlations with Polysomnography-Derived Sleep Parameters. Sleep 38, 853–858 (2015).
pubmed: 26163465
pmcid: 4434551
Barger, L. K. et al. Prevalence of sleep deficiency and use of hypnotic drugs in astronauts before, during, and after spaceflight: an observational study. Lancet Neurol. 13, 904–912 (2014).
pubmed: 25127232
pmcid: 4188436
doi: 10.1016/S1474-4422(14)70122-X
Jones, C. W., Basner, M., Mollicone, D. J., Mott, C. M. & Dinges, D. F. Sleep deficiency in spaceflight is associated with degraded neurobehavioral functions and elevated stress in astronauts on six-month missions aboard the International Space Station. Sleep 45, 1–9 (2022).
doi: 10.1093/sleep/zsac006
Buckey, J. C. in Gravity and the Lung: Lessons from Microgravity (eds G. K. Prisk, J. B. West, & M. Paiva) (Marcel Dekker, 2001).
Buckey, J. C. et al. Microgravity-induced ocular changes are related to body weight. Am. J. Physiol.-Regulatory, Integr. Comp. Physiol. 315, R496–R499 (2018).
doi: 10.1152/ajpregu.00086.2018
Laurie, S. S. et al. Unchanged cerebrovascular CO(2) reactivity and hypercapnic ventilatory response during strict head-down tilt bed rest in a mild hypercapnic environment. J. Physiol. 598, 2491–2505 (2020).
pubmed: 32196672
doi: 10.1113/JP279383
Piantino, J. et al. Link between Mild Traumatic Brain Injury, Poor Sleep, and Magnetic Resonance Imaging: Visible Perivascular Spaces in Veterans. J. Neurotrauma 38, 2391–2399 (2021).
pubmed: 33599176
pmcid: 8390772
doi: 10.1089/neu.2020.7447
Wu, D. et al. Insulin Resistance Is Independently Associated With Enlarged Perivascular Space in the Basal Ganglia in Nondiabetic Healthy Elderly Population. Am. J. Alzheimers Dis. Other Demen 35, 1–6 (2020).
doi: 10.1177/1533317520912126
Martinez-Ramirez, S. et al. Topography of dilated perivascular spaces in subjects from a memory clinic cohort. Neuology 80, 1551–1556 (2013).
Potter, G. M. et al. Enlarged perivascular spaces and cerebral small vessel disease. Int J. Stroke 10, 376–381 (2015).
pubmed: 23692610
doi: 10.1111/ijs.12054
Boespflug, E. L. et al. Targeted Assessment of Enlargement of the Perivascular Space in Alzheimer’s Disease and Vascular Dementia Subtypes Implicates Astroglial Involvement Specific to Alzheimer’s Disease. J. Alzheimers Dis. 66, 1587–1597 (2018).
pubmed: 30475760
pmcid: 6360949
doi: 10.3233/JAD-180367
Gertje, E. C., van Westen, D., Panizo, C., Mattsson-Carlgren, N. & Hansson, O. Association of Enlarged Perivascular Spaces and Measures of Small Vessel and Alzheimer Disease. Neurology 96, e193–e202 (2021).
pubmed: 33046608
doi: 10.1212/WNL.0000000000011046
Lynch, M. et al. Perivascular spaces as a potential biomarker of Alzheimer’s disease. Front Neurosci. 16, 1–16 (2022).
doi: 10.3389/fnins.2022.1021131
Taniguchi, D., Shimura, H., Watanabe, M., Hattori, N. & Urabe, T. Widespread enlarged perivascular spaces associated with dementia and focal brain dysfunction: case report. BMC Neurol. 17, 1–4 (2017).
doi: 10.1186/s12883-017-0997-9
Greenwald, S. H. et al. Intraocular pressure and choroidal thickness respond differently to lower body negative pressure during spaceflight. J. Appl Physiol. (1985) 131, 613–620 (2021).
pubmed: 34166098
doi: 10.1152/japplphysiol.01040.2020
Taoka, T. & Naganawa, S. Glymphatic imaging using MRI. J. Magn. Reson Imaging 51, 11–24 (2020).
pubmed: 31423710
doi: 10.1002/jmri.26892
Meck, J. V., Dreyer, S. A. & Warren, L. E. Long-duration head-down bed rest: project overview, vital signs, and fluid balance. Aviat. Space Environ. Med. 80, A1–A8 (2009).
pubmed: 19476163
doi: 10.3357/ASEM.BR01.2009
Cassady, K. et al. Effects of a spaceflight analog environment on brain connectivity and behavior. Neuroimage 141, 18–30 (2016).
pubmed: 27423254
doi: 10.1016/j.neuroimage.2016.07.029
Marshall-Goebel, K. et al. Effects of short-term exposure to head-down tilt on cerebral hemodynamics: a prospective evaluation of a spaceflight analog using phase-contrast MRI. J. Appl Physiol. 120, 1466–1473 (2016).
pubmed: 27013606
pmcid: 4909835
doi: 10.1152/japplphysiol.00841.2015
Yuan, P. et al. Increased Brain Activation for Dual Tasking with 70-Days Head-Down Bed Rest. Front Syst. Neurosci. 10, 1–14 (2016).
doi: 10.3389/fnsys.2016.00071
Patel, Z. S. et al. Red risks for a journey to the red planet: The highest priority human health risks for a mission to Mars. NPJ Microgravity 6, 1–13 (2020).
doi: 10.1038/s41526-020-00124-6
Schwartz, D. L. et al. Autoidentification of perivascular spaces in white matter using clinical field strength T1 and FLAIR MR imaging. Neuroimage 202, 1–6 (2019).
doi: 10.1016/j.neuroimage.2019.116126
McGregor, H. R. et al. Impacts of spaceflight experience on human brain structure. Sci. Rep. 13, 1–11 (2023).
doi: 10.1038/s41598-023-33331-8
Buis, A. The Atmosphere: Getting a Handle on Carbon Dioxide, https://climate.nasa.gov/news/2915/the-atmosphere-getting-a-handle-on-carbon-dioxide/#:~:text=What%E2%80%99s%20in%20the%20Air%3F&text=By%20volume%2C%20the%20dry%20air,methane%2C%20nitrous%20oxide%20and%20ozone (2019).
Hupfeld, K. E. et al. Neural Correlates of Vestibular Processing During a Spaceflight Analog With Elevated Carbon Dioxide (CO2): A Pilot Study. Front Syst. Neurosci. 13, 1–21 (2019).
McGregor, H. R. et al. Brain connectivity and behavioral changes in a spaceflight analog environment with elevated CO2. Neuroimage 225, 117450 (2020).
pubmed: 33075558
doi: 10.1016/j.neuroimage.2020.117450
Salazar, A. P. et al. Neural Working Memory Changes During a Spaceflight Analog With Elevated Carbon Dioxide: A Pilot Study. Front Syst. Neurosci. 14, 1–15 (2020).
doi: 10.3389/fnsys.2020.00048
Piantino, J. et al. Characterization of MR Imaging-Visible Perivascular Spaces in the White Matter of Healthy Adolescents at 3T. AJNR Am. J. Neuroradiol. 41, 2139–2145 (2020).
pubmed: 33033050
pmcid: 7658833
doi: 10.3174/ajnr.A6789
Smith, S. M. Fast robust automated brain extraction. Hum. Brain Mapp. 17, 143–155 (2002).
pubmed: 12391568
pmcid: 6871816
doi: 10.1002/hbm.10062
Leemans, A., Jeurissen, B. & Sijbers, J. in 17th Annual Meeting of Intl Soc Mag Reson Med. (Hawaii, USA, 2009).
Smith, S. M. et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23, S208–S219 (2004).
pubmed: 15501092
doi: 10.1016/j.neuroimage.2004.07.051
Jenkinson, M., Beckmann, C. F., Behrens, T. E., Woolrich, M. W., & Smith, S.M. Fsl. Neuroimage 62, 782–790 (2012).
pubmed: 21979382
doi: 10.1016/j.neuroimage.2011.09.015
Avants, B. B. et al. The optimal template effect in hippocampus studies of diseased populations. Neuroimage 49, 2457–2466 (2010).
pubmed: 19818860
doi: 10.1016/j.neuroimage.2009.09.062
Avants, B. B. et al. A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage 54, 2033–2044 (2011).
pubmed: 20851191
doi: 10.1016/j.neuroimage.2010.09.025
Jenkinson, M., Bannister, P., Brady, M. & Smith, S. Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images. NeuroImage 17, 825–841 (2002).
pubmed: 12377157
doi: 10.1006/nimg.2002.1132
Tax, C. M. W., Vos, S. B. & Leemans, A. in Diffusion Tensor Imaging Ch. Chapter 7, 127–150 (2016).
Vos, S. B. et al. The importance of correcting for signal drift in diffusion MRI. Magn. Reson Med. 77, 285–299 (2017).
pubmed: 26822700
doi: 10.1002/mrm.26124
Perrone, D. et al. The effect of Gibbs ringing artifacts on measures derived from diffusion MRI. Neuroimage 120, 441–455 (2015).
pubmed: 26142273
doi: 10.1016/j.neuroimage.2015.06.068
Leemans, A. & Jones, D. K. The B-matrix must be rotated when correcting for subject motion in DTI data. Magn. Reson Med. 61, 1336–1349 (2009).
pubmed: 19319973
doi: 10.1002/mrm.21890
Huang, H. et al. Correction of B0 susceptibility induced distortion in diffusion-weighted images using large-deformation diffeomorphic metric mapping. Magn. Reson Imaging 26, 1294–1302 (2008).
pubmed: 18499384
pmcid: 2612638
doi: 10.1016/j.mri.2008.03.005
Lee, A. G., Mader, T. H., Gibson, C. R. & Tarver, W. Space Flight-Associated Neuro-ocular Syndrome. JAMA Ophthalmol. 135, 992–994 (2017).
pubmed: 28727859
doi: 10.1001/jamaophthalmol.2017.2396
Saville, D. J. Multiple comparison procedures: The practical solution. Am. State 44, 174–180 (1990).
Rothman, K. J. No Adjustments Are Needed for Multiple Comparisons. Epidemiology 1, 43–46 (1990).
pubmed: 2081237
doi: 10.1097/00001648-199001000-00010