The effect of optic neuritis attacks on choroidal vascularity index in patients with multiple sclerosis.
Binarization
EDI-optical coherence tomography
choroidal vascularity index
luminal area
multiple sclerosis
Journal
Graefe's archive for clinical and experimental ophthalmology = Albrecht von Graefes Archiv fur klinische und experimentelle Ophthalmologie
ISSN: 1435-702X
Titre abrégé: Graefes Arch Clin Exp Ophthalmol
Pays: Germany
ID NLM: 8205248
Informations de publication
Date de publication:
Aug 2021
Aug 2021
Historique:
received:
08
10
2020
accepted:
02
03
2021
revised:
06
02
2021
pubmed:
26
3
2021
medline:
19
8
2021
entrez:
25
3
2021
Statut:
ppublish
Résumé
To investigate the changes in the choroidal vascularity index (CVI) of patients with multiple sclerosis (MS) using binarization on enhanced depth imaging optical coherence tomography (EDI-OCT) images and to evaluate the effect of optic neuritis (ON) attacks on these measurements. Three groups were created by including forty eyes of 20 patients diagnosed with relapsing-remitting MS and had a unilateral history of ON attack and the randomly selected eyes of 30 healthy age- and sex-matched control subjects. Group 1 (n = 20) consisted of the ON-affected eyes of the MS patients (MSON); group 2 (n = 20) included their fellow healthy eyes (MSNON); group 3 (n = 30) included the eyes of healthy controls. The mean age was 33.3 ± 9.4 years in the MS group and 33.4 ± 11.1 years in the healthy control group. Mean choroidal vascularity index (CVI) was significantly lower in the MSON group than the MSNON group (59.6 ± 3.72 % vs 61.7 ± 3.16 %, p = 0.007). The CVI values of both the MSON and MSNON groups were significantly lower when compared to the controls (63.9 ± 2.76) (p < 0.001, p = 0.030). Compared to controls, the subfoveal total choroidal area and luminal area values were significantly greater in the MSON (p = 0.009, p = 0.009, respectively) and MSNON groups (p = 0.031, p = 0.013, respectively). The presented study demonstrates that, compared to healthy subjects, CVI values are lower in the affected and unaffected eyes of patients who had a history of ON in relation with their MS diagnosis. The presence of significant anatomical changes, especially in the luminal area, may suggest that ON causes vascular disorganization which contributes to MS pathophysiology.
Identifiants
pubmed: 33763732
doi: 10.1007/s00417-021-05143-x
pii: 10.1007/s00417-021-05143-x
doi:
Types de publication
Clinical Trial
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2413-2424Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
National Multiple Sclerosis Society (2020) New York: Who gest MS (epidemiology); [cited 2020 March 20]. Available from: http://www.nationalmssociety.org/What-is-MS/Who-Gets-MS
Lublin FD, Reingold SC (1996) Defining the clinical course of multiple sclerosis: results of an international survey. National Multiple Sclerosis Society (USA) Advisory Committee on Clinical Trials of New Agents in Multiple Sclerosis. Neurology 46(4):907–911. https://doi.org/10.1212/wnl.46.4.907
doi: 10.1212/wnl.46.4.907
pubmed: 8780061
Multiple sclerosis risk after optic neuritis: final optic neuritis treatment trial follow-up (2008) Arch Neurol 65(6):727-732. doi:10.1001/archneur.65.6.727
McFarland HF, Martin R (2007) Multiple sclerosis: a complicated picture of autoimmunity. Nat Immunol 8(9):913–919. https://doi.org/10.1038/ni1507.
doi: 10.1038/ni1507.
pubmed: 17712344
Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mörk S, Bö L (1998) Axonal transection in the lesions of multiple sclerosis. N Engl J Med 338(5):278–285. https://doi.org/10.1056/nejm199801293380502.
doi: 10.1056/nejm199801293380502.
pubmed: 9445407
Costello F, Hodge W, Pan YI, Eggenberger E, Coupland S, Kardon RH (2008) Tracking retinal nerve fiber layer loss after optic neuritis: a prospective study using optical coherence tomography. Mult Scler 14(7):893–905. https://doi.org/10.1177/1352458508091367.
doi: 10.1177/1352458508091367.
pubmed: 18573837
Ratchford JN, Saidha S, Sotirchos ES, Oh JA, Seigo MA, Eckstein C et al (2013) Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning. Neurology 80(1):47–54. https://doi.org/10.1212/WNL.0b013e31827b1a1c.
doi: 10.1212/WNL.0b013e31827b1a1c.
pubmed: 23267030
pmcid: 3589201
Akarsu C, Tan FU, Kendi T (2004) Color Doppler imaging in optic neuritis with multiple sclerosis. Graefes Arch Clin Exp Ophthalmol 242(12):990–994. https://doi.org/10.1007/s00417-004-0948-1.
doi: 10.1007/s00417-004-0948-1.
pubmed: 15592867
Modrzejewska M, Karczewicz D, Wilk G (2007) Assessment of blood flow velocity in eyeball arteries in multiple sclerosis patients with past retrobulbar optic neuritis in color Doppler ultrasonography. Klin Ocz 109(4-6):183–186
Pache M, Kaiser HJ, Akhalbedashvili N, Lienert C, Dubler B, Kappos L, Flammer J (2003) Extraocular blood flow and endothelin-1 plasma levels in patients with multiple sclerosis. Eur Neurol 49(3):164–168. https://doi.org/10.1159/000069085.
doi: 10.1159/000069085.
pubmed: 12646761
Ingegnoli F, Gualtierotti R, Pierro L, Del Turco C, Miserocchi E, Schioppo T, Meroni PL (2015) Choroidal impairment and macular thinning in patients with systemic sclerosis: the acute study. Microvasc Res 97:31–36. https://doi.org/10.1016/j.mvr.2014.08.008.
doi: 10.1016/j.mvr.2014.08.008.
pubmed: 25262916
Kim M, Kim SS, Kwon HJ, Koh HJ, Lee SC (2012) Association between choroidal thickness and ocular perfusion pressure in young, healthy subjects: enhanced depth imaging optical coherence tomography study. Invest Ophthalmol Vis Sci 53(12):7710–7717
doi: 10.1167/iovs.12-10464
Novais EA, Badaró E, Allemann N, Morales MS, Rodrigues EB, de Souza Lima R, Regatieri CV, Belfort R Jr (2015) Correlation Between Choroidal Thickness and Ciliary Artery Blood Flow Velocity in Normal Subjects. Ophthalmic Surg Lasers Imaging Retina 46(9):920–924. https://doi.org/10.3928/23258160-20151008-04.
doi: 10.3928/23258160-20151008-04.
pubmed: 26469231
Sonoda S, Sakamoto T, Yamashita T, Shirasawa M, Uchino E, Terasaki H, Tomita M (2014) Choroidal structure in normal eyes and after photodynamic therapy determined by binarization of optical coherence tomographic images. Invest Ophthalmol Vis Sci 55(6):3893–3899. https://doi.org/10.1167/iovs.14-14447
doi: 10.1167/iovs.14-14447
pubmed: 24894395
Agrawal R, Gupta P, Tan KA, Cheung CM, Wong TY, Cheng CY (2016) Choroidal vascularity index as a measure of vascular status of the choroid: Measurements in healthy eyes from a population-based study. Sci Rep 6:21090. https://doi.org/10.1038/srep21090.
doi: 10.1038/srep21090.
pubmed: 26868048
pmcid: 4751574
Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M et al (2011) Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol 69(2):292–302. https://doi.org/10.1002/ana.22366
doi: 10.1002/ana.22366
pubmed: 21387374
pmcid: 3084507
Hayreh SS (1969) Blood supply of the optic nerve head and its role in optic atrophy, glaucoma, and oedema of the optic disc. Br J Ophthalmol 53(11):721–748. https://doi.org/10.1136/bjo.53.11.721.
doi: 10.1136/bjo.53.11.721.
pubmed: 4982590
pmcid: 506749
Kur J, Newman EA, Chan-Ling T (2012) Cellular and physiological mechanisms underlying blood flow regulation in the retina and choroid in health and disease. Prog Retin Eye Res 31(5):377–406. https://doi.org/10.1016/j.preteyeres.2012.04.004
doi: 10.1016/j.preteyeres.2012.04.004
pubmed: 22580107
pmcid: 3418965
Linsenmeier RA, Padnick-Silver L (2000) Metabolic dependence of photoreceptors on the choroid in the normal and detached retina. Invest Ophthalmol Vis Sci 41(10):3117–3123
pubmed: 10967072
Spaide RF, Koizumi H, Pozzoni MC (2008) Enhanced depth imaging spectral-domain optical coherence tomography. Am J Ophthalmol 146(4):496–500. https://doi.org/10.1016/j.ajo.2008.05.032.
doi: 10.1016/j.ajo.2008.05.032.
pubmed: 18639219
Doğan Ü, Ulaş F, Türkoğlu ŞA, Ögün MN, Ağca S (2019) Eyes are mirror of the brain: comparison of multiple sclerosis patients and healthy controls using OCT. Int J Neurosci 129(9):848–855. https://doi.org/10.1080/00207454.2019.1576660
doi: 10.1080/00207454.2019.1576660
pubmed: 30696321
Esen E, Sizmaz S, Demir T, Demirkiran M, Unal I, Demircan N (2016) Evaluation of Choroidal Vascular Changes in Patients with Multiple Sclerosis Using Enhanced Depth Imaging Optical Coherence Tomography. Ophthalmologica 235(2):65–71. https://doi.org/10.1159/000441152.
doi: 10.1159/000441152.
pubmed: 26485541
Gordon-Lipkin E, Chodkowski B, Reich DS, Smith SA, Pulicken M, Balcer LJ, Frohman EM, Cutter G, Calabresi PA (2007) Retinal nerve fiber layer is associated with brain atrophy in multiple sclerosis. Neurology 69(16):1603–1609. https://doi.org/10.1212/01.wnl.0000295995.46586.ae
doi: 10.1212/01.wnl.0000295995.46586.ae
pubmed: 17938370
Adhya S, Johnson G, Herbert J, Jaggi H, Babb JS, Grossman RI, Inglese M (2006) Pattern of hemodynamic impairment in multiple sclerosis: dynamic susceptibility contrast perfusion MR imaging at 3. 0 T Neuroimage 33(4):1029–1035
doi: 10.1016/j.neuroimage.2006.08.008
Law M, Saindane AM, Ge Y, Babb JS, Johnson G, Mannon LJ, Herbert J, Grossman RI (2004) Microvascular abnormality in relapsing-remitting multiple sclerosis: perfusion MR imaging findings in normal-appearing white matter. Radiology 231(3):645–652. https://doi.org/10.1148/radiol.2313030996.
doi: 10.1148/radiol.2313030996.
pubmed: 15163806
Haufschild T, Shaw SG, Kesselring J, Flammer J (2001) Increased endothelin-1 plasma levels in patients with multiple sclerosis. J Neuroophthalmol 21(1):37–38. https://doi.org/10.1097/00041327-200103000-00011.
doi: 10.1097/00041327-200103000-00011.
pubmed: 11315981
D'Haeseleer M, Beelen R, Fierens Y, Cambron M, Vanbinst AM, Verborgh C, Demey J, De Keyser J (2013) Cerebral hypoperfusion in multiple sclerosis is reversible and mediated by endothelin-1. Proc Natl Acad Sci U S A 110(14):5654–5658. https://doi.org/10.1073/pnas.1222560110
doi: 10.1073/pnas.1222560110
pubmed: 23509249
pmcid: 3619305
Cambron M, D'haeseleer M, Laureys G, Clinckers R, Debruyne J, De Keyser J (2012) White-matter astrocytes, axonal energy metabolism, and axonal degeneration in multiple sclerosis. J Cereb Blood Flow Metab 32(3):413–424
doi: 10.1038/jcbfm.2011.193
Trapp BD, Stys PK (2009) Virtual hypoxia and chronic necrosis of demyelinated axons in multiple sclerosis. Lancet Neurol 8(3):280–291. https://doi.org/10.1016/s1474-4422(09)70043-2.
doi: 10.1016/s1474-4422(09)70043-2.
pubmed: 19233038
Blomstrand F, Giaume C (2006) Kinetics of endothelin-induced inhibition and glucose permeability of astrocyte gap junctions. J Neurosci Res 83(6):996–1003. https://doi.org/10.1002/jnr.20801.
doi: 10.1002/jnr.20801.
pubmed: 16609958
Chen TC, Yeh CY, Lin CW, Yang CM, Yang CH, Lin IH, Chen PY, Cheng JY, Hu FR (2017) Vascular hypoperfusion in acute optic neuritis is a potentially new neurovascular model for demyelinating diseases. PLoS One 12(9):e0184927. https://doi.org/10.1371/journal.pone.0184927.
doi: 10.1371/journal.pone.0184927.
pubmed: 28926646
pmcid: 5605049
Wang X, Jia Y, Spain R, Potsaid B, Liu JJ, Baumann B, Hornegger J, Fujimoto JG, Wu Q, Huang D (2014) Optical coherence tomography angiography of optic nerve head and parafovea in multiple sclerosis. Br J Ophthalmol 98(10):1368–1373. https://doi.org/10.1136/bjophthalmol-2013-304547
doi: 10.1136/bjophthalmol-2013-304547
pubmed: 24831719
Han JM, Hwang JM, Kim JS, Park KH, Woo SJ (2014) Changes in choroidal thickness after systemic administration of high-dose corticosteroids: a pilot study. Invest Ophthalmol Vis Sci 55(1):440–445. https://doi.org/10.1167/iovs.13-12854.
doi: 10.1167/iovs.13-12854.
pubmed: 24370828
Balk LJ, Petzold A (2014) Current and future potential of retinal optical coherence tomography in multiple sclerosis with and without optic neuritis. Neurodegener Dis Manag 4(2):165–176. https://doi.org/10.2217/nmt.14.10.
doi: 10.2217/nmt.14.10.
pubmed: 24832034
Gelfand JM, Goodin DS, Boscardin WJ, Nolan R, Cuneo A, Green AJ (2012) Retinal axonal loss begins early in the course of multiple sclerosis and is similar between progressive phenotypes. PLoS One 7(5):e36847. https://doi.org/10.1371/journal.pone.0036847.
doi: 10.1371/journal.pone.0036847.
pubmed: 22666330
pmcid: 3359324
Alonso R, Gonzalez-Moron D, Garcea O (2018) Optical coherence tomography as a biomarker of neurodegeneration in multiple sclerosis: A review. Mult Scler Relat Disord 22:77–82. https://doi.org/10.1016/j.msard.2018.03.007.
doi: 10.1016/j.msard.2018.03.007.
pubmed: 29605802
Walter SD, Ishikawa H, Galetta KM, Sakai RE, Feller DJ, Henderson SB et al (2012) Ganglion cell loss in relation to visual disability in multiple sclerosis. Ophthalmology 119(6):1250–1257. https://doi.org/10.1016/j.ophtha.2011.11.032
doi: 10.1016/j.ophtha.2011.11.032
pubmed: 22365058
Trip SA, Schlottmann PG, Jones SJ, Altmann DR, Garway-Heath DF, Thompson AJ, Plant GT, Miller DH (2005) Retinal nerve fiber layer axonal loss and visual dysfunction in optic neuritis. Ann Neurol 58(3):383–391. https://doi.org/10.1002/ana.20575
doi: 10.1002/ana.20575
pubmed: 16075460
Frohman EM, Fujimoto JG, Frohman TC, Calabresi PA, Cutter G, Balcer LJ (2008) Optical coherence tomography: a window into the mechanisms of multiple sclerosis. Nat Clin Pract Neurol 4(12):664–675. https://doi.org/10.1038/ncpneuro0950.
doi: 10.1038/ncpneuro0950.
pubmed: 19043423
pmcid: 2743162
Fisher JB, Jacobs DA, Markowitz CE, Galetta SL, Volpe NJ, Nano-Schiavi ML et al (2006) Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis. Ophthalmology 113(2):324–332. https://doi.org/10.1016/j.ophtha.2005.10.040
doi: 10.1016/j.ophtha.2005.10.040
pubmed: 16406539
Balcer LJ, Miller DH, Reingold SC, Cohen JA (2015) Vision and vision-related outcome measures in multiple sclerosis. Brain 138(1):11–27. https://doi.org/10.1093/brain/awu335.
doi: 10.1093/brain/awu335.
pubmed: 25433914
Klistorner A, Arvind H, Nguyen T, Garrick R, Paine M, Graham S, O'Day J, Yiannikas C (2009) Multifocal VEP and OCT in optic neuritis: a topographical study of the structure-function relationship. Doc Ophthalmol 118(2):129–137. https://doi.org/10.1007/s10633-008-9147-4.
doi: 10.1007/s10633-008-9147-4.
pubmed: 18779985
Martinez-Lapiscina EH, Arnow S, Wilson JA, Saidha S, Preiningerova JL, Oberwahrenbrock T et al (2016) Retinal thickness measured with optical coherence tomography and risk of disability worsening in multiple sclerosis: a cohort study. Lancet Neurol 15(6):574–584. https://doi.org/10.1016/s1474-4422(16)00068-5.
doi: 10.1016/s1474-4422(16)00068-5.
pubmed: 27011339