Investigating the blood-spinal cord barrier in preclinical models: a systematic review of in vivo imaging techniques.


Journal

Spinal cord
ISSN: 1476-5624
Titre abrégé: Spinal Cord
Pays: England
ID NLM: 9609749

Informations de publication

Date de publication:
Jun 2021
Historique:
received: 18 07 2020
accepted: 01 03 2021
revised: 25 02 2021
pubmed: 21 3 2021
medline: 16 10 2021
entrez: 20 3 2021
Statut: ppublish

Résumé

This study is a systematic review. To evaluate current in vivo techniques used in the investigation of the blood-spinal cord barrier (BSCB). Search of English language literature for animal studies that investigated the BSCB in vivo. Data extraction included animal model/type, protocol for BSCB evaluation, and study outcomes. Descriptive syntheses are provided. A total of 40 studies were included, which mainly investigated rodent models of experimental autoimmune encephalomyelitis (EAE) or spinal cord injury (SCI). The main techniques used were magnetic resonance imaging (MRI) and intravital microscopy (IVM). MRI served as a reliable tool to longitudinally track BSCB permeability changes with dynamic contrast enhancement (DCE) using gadolinium, or assess inflammatory infiltrations with targeted alternative contrast agents. IVM provided high-resolution visualization of cellular and molecular interactions across the microvasculature, commonly with either epi-fluorescence or two-photon microscopy. MRI and IVM techniques enabled the evaluation of therapeutic interventions and mechanisms that drive spinal cord dysfunction in EAE and SCI. A small number of studies demonstrated the feasibility of DCE-computed tomography, ultrasound, bioluminescent, and fluorescent optical imaging methods to evaluate the BSCB. Technique-specific limitations and multiple protocols for image acquisition and data analyses are described for all techniques. There are few in vivo investigations of the BSCB. Additional studies are needed in less commonly studied spinal cord disorders, and to establish standardized protocols for data acquisition and analysis. Further development of techniques and multimodal approaches could overcome current imaging limitations to the spinal cord. These advancements might promote wider adoption of techniques, and can provide greater potential for clinical translation.

Identifiants

pubmed: 33742118
doi: 10.1038/s41393-021-00623-7
pii: 10.1038/s41393-021-00623-7
doi:

Types de publication

Journal Article Review Systematic Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

596-612

Subventions

Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (NINDS)
ID : R25NS099008
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (NINDS)
ID : R01NS100459
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (NINDS)
ID : R01NS090904
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (NINDS)
ID : R01NS034467
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Environmental Health Sciences (NIEHS)
ID : R01ES024936
Organisme : U.S. Department of Health & Human Services | NIH | National Institute on Aging (U.S. National Institute on Aging)
ID : P01AG055367 Sub 5202
Organisme : U.S. Department of Health & Human Services | NIH | National Institute on Aging (U.S. National Institute on Aging)
ID : R01AG039452
Organisme : U.S. Department of Health & Human Services | NIH | National Institute on Aging (U.S. National Institute on Aging)
ID : R01AG023084

Références

Bartanusz V, Jezova D, Alajajian B, Digicaylioglu M. The blood-spinal cord barrier: morphology and clinical implications. Ann Neurol. 2011;70:194–206.
pubmed: 21674586 doi: 10.1002/ana.22421
Lutz SE, Smith JR, Kim DH, Olson CVL, Ellefsen K, Bates JM, et al. Caveolin1 is required for Th1 cell infiltration, but not tight junction remodeling, at the blood-brain barrier in autoimmune neuroinflammation. Cell Rep. 2017;21:2104–17.
pubmed: 29166603 pmcid: 5728697 doi: 10.1016/j.celrep.2017.10.094
Sharma HS. Pathophysiology of the blood–spinal cord barrier in traumatic injury. In: Sharma HS, Westman J, editors. Blood-spinal cord and brain barriers in health and disease. San Diego, California: Elsevier Academic Press; 2004. p. 437–518.
Sweeney MD, Zhao Z, Montagne A, Nelson AR, Zlokovic BV. Blood-brain barrier: from physiology to disease and back. Physiol Rev. 2019;99:21–78.
pubmed: 30280653 doi: 10.1152/physrev.00050.2017
Davalos D, Ryu JK, Merlini M, Baeten KM, Le Moan N, Petersen MA, et al. Fibrinogen-induced perivascular microglial clustering is required for the development of axonal damage in neuroinflammation. Nat Commun. 2012;3:1227.
pubmed: 23187627 pmcid: 3514498 doi: 10.1038/ncomms2230
Bilgen M, Dogan B, Narayana PA. In vivo assessment of blood-spinal cord barrier permeability: serial dynamic contrast enhanced MRI of spinal cord injury. Magn Reson Imaging. 2002;20:337–41.
pubmed: 12165352 doi: 10.1016/S0730-725X(02)00504-0
Stirling DP, Liu S, Kubes P, Yong VW. Depletion of Ly6G/Gr-1 leukocytes after spinal cord injury in mice alters wound healing and worsens neurological outcome. J Neurosci. 2009;29:753–64.
pubmed: 19158301 pmcid: 6665178 doi: 10.1523/JNEUROSCI.4918-08.2009
Tang P, Zhang Y, Chen C, Ji X, Ju F, Liu X, et al. In vivo two-photon imaging of axonal dieback, blood flow, and calcium influx with methylprednisolone therapy after spinal cord injury. Sci Rep. 2015;5:9691.
pubmed: 25989524 pmcid: 4437044 doi: 10.1038/srep09691
Borjini N, Paouri E, Tognatta R, Akassoglou K, Davalos D. Imaging the dynamic interactions between immune cells and the neurovascular interface in the spinal cord. Exp Neurol. 2019;322:113046.
pubmed: 31472115 pmcid: 7328885 doi: 10.1016/j.expneurol.2019.113046
Davalos D, Lee JK, Smith WB, Brinkman B, Ellisman MH, Zheng B, et al. Stable in vivo imaging of densely populated glia, axons and blood vessels in the mouse spinal cord using two-photon microscopy. J Neurosci Methods. 2008;169:1–7.
pubmed: 18192022 doi: 10.1016/j.jneumeth.2007.11.011
Haghayegh Jahromi N, Tardent H, Enzmann G, Deutsch U, Kawakami N, Bittner S, et al. A novel cervical spinal cord window preparation allows for two-photon imaging of T-cell interactions with the cervical spinal cord microvasculature during experimental autoimmune encephalomyelitis. Front Immunol. 2017;8:406.
pubmed: 28443093 pmcid: 5387098 doi: 10.3389/fimmu.2017.00406
Figley SA, Chen Y, Maeda A, Conroy L, McMullen JD, Silver JI, et al. A spinal cord window chamber model for in vivo longitudinal multimodal optical and acoustic imaging in a murine model. PLoS One. 2013;8:e58081.
pubmed: 23516432 pmcid: 3597636 doi: 10.1371/journal.pone.0058081
Cheng YT, Lett KM, Schaffer CB. Surgical preparations, labeling strategies, and optical techniques for cell-resolved, in vivo imaging in the mouse spinal cord. Exp Neurol. 2019;318:192–204.
pubmed: 31095935 pmcid: 6588420 doi: 10.1016/j.expneurol.2019.05.010
Hooijmans CR, Ritskes-Hoitinga M. Progress in using systematic reviews of animal studies to improve translational research. PLoS Med. 2013;10:e1001482. https://doi.org/10.1371/journal.pmed.1001482 .
pubmed: 23874162 pmcid: 3712909 doi: 10.1371/journal.pmed.1001482
Watzlawick R, Antonic A, Sena ES, Kopp MA, Rind J, Dirnagl U, et al. Outcome heterogeneity and bias in acute experimental spinal cord injury: a meta-analysis. Neurology. 2019;93:e40–51.
pubmed: 31175207 pmcid: 6659001 doi: 10.1212/WNL.0000000000007718
Aube B, Levesque SA, Pare A, Chamma E, Kebir H, Gorina R, et al. Neutrophils mediate blood-spinal cord barrier disruption in demyelinating neuroinflammatory diseases. J Immunol. 2014;193:2438–54.
pubmed: 25049355 doi: 10.4049/jimmunol.1400401
Bartholomaus I, Kawakami N, Odoardi F, Schlager C, Miljkovic D, Ellwart JW, et al. Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature. 2009;462:94–8.
pubmed: 19829296 doi: 10.1038/nature08478
Bendszus M, Ladewig G, Jestaedt L, Misselwitz B, Solymosi L, Toyka K, et al. Gadofluorine M enhancement allows more sensitive detection of inflammatory CNS lesions than T2-w imaging: a quantitative MRI study. Brain. 2008;131:2341–52.
pubmed: 18669504 doi: 10.1093/brain/awn156
Berens SA, Colvin DC, Yu CG, Yezierski RP, Mareci TH. Evaluation of the pathologic characteristics of excitotoxic spinal cord injury with MR imaging. AJNR Am J Neuroradiol. 2005;26:1612–22.
pubmed: 16091503 pmcid: 7975169
Bilgen M, Abbe R, Narayana PA. Dynamic contrast-enhanced MRI of experimental spinal cord injury: in vivo serial studies. Magn Reson Med. 2001;45:614–22.
pubmed: 11283989 doi: 10.1002/mrm.1083
Bilgen M, Narayana PA. A pharmacokinetic model for quantitative evaluation of spinal cord injury with dynamic contrast-enhanced magnetic resonance imaging. Magn Reson Med. 2001;46:1099–106.
pubmed: 11746575 doi: 10.1002/mrm.1305
Byrnes KR, Fricke ST, Faden AI. Neuropathological differences between rats and mice after spinal cord injury. J Magn Reson Imaging. 2010;32:836–46.
pubmed: 20882614 pmcid: 2949295 doi: 10.1002/jmri.22323
Cahill LS, Laliberte CL, Liu XJ, Bishop J, Nieman BJ, Mogil JS, et al. Quantifying blood-spinal cord barrier permeability after peripheral nerve injury in the living mouse. Mol Pain. 2014;10:60.
pubmed: 25216623 pmcid: 4190293 doi: 10.1186/1744-8069-10-60
Cohen DM, Patel CB, Ahobila-Vajjula P, Sundberg LM, Chacko T, Liu SJ, et al. Blood-spinal cord barrier permeability in experimental spinal cord injury: dynamic contrast-enhanced MRI. NMR Biomed. 2009;22:332–41.
pubmed: 19023867 pmcid: 2741317 doi: 10.1002/nbm.1343
Dray C, Rougon G, Debarbieux F. Quantitative analysis by in vivo imaging of the dynamics of vascular and axonal networks in injured mouse spinal cord. Proc Natl Acad Sci USA. 2009;106:9459–64.
pubmed: 19470644 doi: 10.1073/pnas.0900222106
Eaton VL, Vasquez KO, Goings GE, Hunter ZN, Peterson JD, Miller SD. Optical tomographic imaging of near infrared imaging agents quantifies disease severity and immunomodulation of experimental autoimmune encephalomyelitis in vivo. J Neuroinflammation. 2013;10:138.
pubmed: 24237884 pmcid: 4225609 doi: 10.1186/1742-2094-10-138
Fournier AP, Quenault A, Martinez de Lizarrondo S, Gauberti M, Defer G, Vivien D, et al. Prediction of disease activity in models of multiple sclerosis by molecular magnetic resonance imaging of P-selectin. Proc Natl Acad Sci USA. 2017;114:6116–21.
pubmed: 28533365 doi: 10.1073/pnas.1619424114
Herrera JJ, Sundberg LM, Zentilin L, Giacca M, Narayana PA. Sustained expression of vascular endothelial growth factor and angiopoietin-1 improves blood-spinal cord barrier integrity and functional recovery after spinal cord injury. J Neurotrauma. 2010;27:2067–76.
pubmed: 20799882 pmcid: 2978057 doi: 10.1089/neu.2010.1403
Kang CE, Clarkson R, Tator CH, Yeung IW, Shoichet MS. Spinal cord blood flow and blood vessel permeability measured by dynamic computed tomography imaging in rats after localized delivery of fibroblast growth factor. J Neurotrauma. 2010;27:2041–53.
pubmed: 20799884 doi: 10.1089/neu.2010.1345
Ladewig G, Jestaedt L, Misselwitz B, Solymosi L, Toyka K, Bendszus M, et al. Spatial diversity of blood-brain barrier alteration and macrophage invasion in experimental autoimmune encephalomyelitis: a comparative MRI study. Exp Neurol. 2009;220:207–11.
pubmed: 19733560 doi: 10.1016/j.expneurol.2009.08.027
Locatelli G, Theodorou D, Kendirli A, Jordao MJC, Staszewski O, Phulphagar K, et al. Mononuclear phagocytes locally specify and adapt their phenotype in a multiple sclerosis model. Nat Neurosci. 2018;21:1196–208.
pubmed: 30127427 doi: 10.1038/s41593-018-0212-3
Odoardi F, Sie C, Streyl K, Ulaganathan VK, Schlager C, Lodygin D, et al. T cells become licensed in the lung to enter the central nervous system. Nature. 2012;488:675–9.
pubmed: 22914092 doi: 10.1038/nature11337
Patel CB, Cohen DM, Ahobila-Vajjula P, Sundberg LM, Chacko T, Narayana PA. Effect of VEGF treatment on the blood-spinal cord barrier permeability in experimental spinal cord injury: dynamic contrast-enhanced magnetic resonance imaging. J Neurotrauma. 2009;26:1005–16.
pubmed: 19226205 pmcid: 2857512 doi: 10.1089/neu.2008.0860
Sathiyanadan K, Coisne C, Enzmann G, Deutsch U, Engelhardt B. PSGL-1 and E/P-selectins are essential for T-cell rolling in inflamed CNS microvessels but dispensable for initiation of EAE. Eur J Immunol. 2014;44:2287–94.
pubmed: 24740164 doi: 10.1002/eji.201344214
Schellenberg AE, Buist R, Yong VW, Del Bigio MR, Peeling J. Magnetic resonance imaging of blood-spinal cord barrier disruption in mice with experimental autoimmune encephalomyelitis. Magn Reson Med. 2007;58:298–305.
pubmed: 17654586 doi: 10.1002/mrm.21289
Soubeyrand M, Badner A, Vawda R, Chung YS, Fehlings MG. Very high resolution ultrasound imaging for real-time quantitative visualization of vascular disruption after spinal cord injury. J Neurotrauma. 2014;31:1767–75.
pubmed: 24831774 pmcid: 4186763 doi: 10.1089/neu.2013.3319
Tatar I, Chou PC, Desouki MM, El Sayed H, Bilgen M. Evaluating regional blood spinal cord barrier dysfunction following spinal cord injury using longitudinal dynamic contrast-enhanced MRI. BMC Med Imaging. 2009;9:10.
pubmed: 19519898 pmcid: 2714086 doi: 10.1186/1471-2342-9-10
Vajkoczy P, Laschinger M, Engelhardt B. Alpha4-integrin-VCAM-1 binding mediates G protein-independent capture of encephalitogenic T cell blasts to CNS white matter microvessels. J Clin Invest. 2001;108:557–65.
pubmed: 11518729 pmcid: 209399 doi: 10.1172/JCI12440
Yasuda K, Cline C, Lin YS, Scheib R, Ganguly S, Thirumaran RK, et al. In vivo imaging of human MDR1 transcription in the brain and spine of MDR1-luciferase reporter mice. Drug Metab Dispos. 2015;43:1646–54.
pubmed: 26281846 pmcid: 4613952 doi: 10.1124/dmd.115.065078
Tofts PS, Brix G, Buckley DL, Evelhoch JL, Henderson E, Knopp MV, et al. Estimating kinetic parameters from dynamic contrast-enhanced T(1)-weighted MRI of a diffusable tracer: standardized quantities and symbols. J Magn Reson Imaging. 1999;10:223–32.
pubmed: 10508281 doi: 10.1002/(SICI)1522-2586(199909)10:3<223::AID-JMRI2>3.0.CO;2-S
Weller RO, Sharp MM, Christodoulides M, Carare RO, Mollgard K. The meninges as barriers and facilitators for the movement of fluid, cells and pathogens related to the rodent and human CNS. Acta Neuropathol. 2018;135:363–85.
pubmed: 29368214 doi: 10.1007/s00401-018-1809-z
Cuvinciuc V, Viallon M, Barnaure I, Vargas MI, Lovblad KO, Haller S. Dynamic contrast-enhanced MR perfusion of intradural spinal lesions. AJNR Am J Neuroradiol. 2017;38:192–4.
pubmed: 27856434 pmcid: 7963642 doi: 10.3174/ajnr.A4995
Bisdas S, Rumboldt Z, Surlan K, Koh TS, Deveikis J, Spampinato MV. Perfusion CT measurements in healthy cervical spinal cord: feasibility and repeatability of the study as well as interchangeability of the perfusion estimates using two commercially available software packages. Eur Radiol. 2008;18:2321–8.
pubmed: 18431576 doi: 10.1007/s00330-008-0973-2
Fisher DT, Muhitch JB, Kim M, Doyen KC, Bogner PN, Evans SS, et al. Intraoperative intravital microscopy permits the study of human tumour vessels. Nat Commun. 2016;7:10684.
pubmed: 26883450 pmcid: 4757793 doi: 10.1038/ncomms10684
Rennert RC, Strickland BA, Ravina K, Bakhsheshian J, Fredrickson V, Carey J, et al. Intraoperative assessment of cortical perfusion after intracranial-to-intracranial and extracranial-to-intracranial bypass for complex cerebral aneurysms using Flow 800. Oper Neurosurg (Hagerstown). 2019;16:583–92.
doi: 10.1093/ons/opy154

Auteurs

Joshua Bakhsheshian (J)

Department of Neurological Surgery, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA. joshuabakh@gmail.com.

Ben A Strickland (BA)

Department of Neurological Surgery, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.

William J Mack (WJ)

Department of Neurological Surgery, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.

Berislav V Zlokovic (BV)

Department of Physiology and Neuroscience, The Zilkha Neurogenetic Institute, Keck School of Medicine of the University of Southern California, Los Angeles, CA, USA.

Articles similaires

Humans Ketamine Propofol Pulmonary Atelectasis Female
Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Photosynthesis Ribulose-Bisphosphate Carboxylase Carbon Dioxide Molecular Dynamics Simulation Cyanobacteria

Classifications MeSH