Advertisement
Review Article| Volume 30, ISSUE 7, 105828, July 2021

Download started.

Ok

Structural and Functional Imaging of the Retina in Central Retinal Artery Occlusion – Current Approaches and Future Directions

      Abstract

      Central retinal artery occlusion (CRAO) is a form of acute ischemic stroke which affects the retina. Intravenous thrombolysis is emerging as a compelling therapeutic approach. However, it is not known which patients may benefit from this therapy because there are no imaging modalities that adequately distinguish viable retina from irreversibly infarcted retina. The inner retina receives arterial supply from the central retinal artery and there is robust collateralization between this circulation and the outer retinal circulation, provided by the posterior ciliary circulation. Fundus photography can show canonical changes associated with CRAO including a cherry-red spot, arteriolar boxcarring and retinal pallor. Fluorescein angiography provides 2-dimensional imaging of the retinal circulation and can distinguish a complete from a partial CRAO as well as central versus peripheral retinal non-perfusion. Transorbital ultrasonography may assay flow through the central retinal artery and is useful in the exclusion of other orbital pathology that can mimic CRAO. Optical coherence tomography provides structural information on the different layers of the retina and exploratory work has described its utility in determining the time since onset of ischemia. Two experimental techniques are discussed. 1) Retinal functional imaging permits generation of capillary perfusion maps and can assay retinal oxygenation and blood flow velocity. 2) Photoacoustic imaging combines the principles of optical excitation and ultrasonic detection and - in animal studies - has been used to determine the retinal oxygen metabolic rate. Future techniques to determine retinal viability in clinical practice will require rapid, easily used, and reproducible methods that can be deployed in the emergency setting.

      Key Words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of Stroke and Cerebrovascular Diseases
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      Referenecs

        • Sacco RL
        • Kasner SE
        • Broderick JP
        • Caplan LR
        • Connors JJ
        • Culebras A
        • et al.
        An updated definition of stroke for the 21st century: a statement for healthcare professionals from the american heart association/american stroke association.
        Stroke. 2013; 44: 2064-2089
        • Scott IU
        • Campochiaro PA
        • Newman NJ
        • Biousse V.
        Retinal vascular occlusions.
        Lancet. 2020; 396: 1927-1940
        • Schrag M
        • Youn T
        • Schindler J
        • Kirshner H
        • Greer D.
        Intravenous fibrinolytic therapy in central retinal artery occlusion: a patient-level meta-analysis.
        JAMA Neurol. 2015; 72: 1148-1154
        • Thomalla G
        • Simonsen CZ
        • Boutitie F
        • Andersen G
        • Berthezene Y
        • Cheng B
        • et al.
        Mri-guided thrombolysis for stroke with unknown time of onset.
        N Engl J Med. 2018; 379: 611-622
        • Nogueira RG
        • Jadhav AP
        • Haussen DC
        • Bonafe A
        • Budzik RF
        • Bhuva P
        • et al.
        Thrombectomy 6 to 24 hours after stroke with a mismatch between deficit and infarct.
        N Engl J Med. 2018; 378: 11-21
        • Albers GW
        • Marks MP
        • Kemp S
        • Christensen S
        • Tsai JP
        • Ortega-Gutierrez S
        • et al.
        Thrombectomy for stroke at 6 to 16 hours with selection by perfusion imaging.
        N Engl J Med. 2018; 378: 708-718
        • Flaxel CJ
        • Adelman RA
        • Bailey ST
        • Fawzi A
        • Lim JI
        • Vemulakonda GA
        • et al.
        Retinal and ophthalmic artery occlusions preferred practice pattern®.
        Ophthalmology. 2020; 127: P259-P287
        • Powers WJ
        • Rabinstein AA
        • Ackerson T
        • Adeoye OM
        • Bambakidis NC
        • Becker K
        • et al.
        Guidelines for the early management of patients with acute ischemic stroke: 2019 update to the 2018 guidelines for the early management of acute ischemic stroke: a guideline for healthcare professionals from the american heart association/american stroke association.
        Stroke. 2019; 50 (e344-e418)
        • Mac Grory B
        • Nackenoff A
        • Poli S
        • Spitzer MS
        • Nedelmann M
        • Guillon B
        • et al.
        Intravenous fibrinolysis for central retinal artery occlusion: a cohort study and updated patient-level meta-analysis.
        Stroke. 2020; 51: 2018-2025
        • Khatri P
        • Kleindorfer DO
        • Devlin T
        • Sawyer RN
        • Starr M
        • Mejilla J
        • et al.
        Effect of alteplase vs aspirin on functional outcome for patients with acute ischemic stroke and minor nondisabling neurologic deficits: The prisms randomized clinical trial.
        JAMA. 2018; 320: 156-166
        • Fallico M
        • Lotery AJ
        • Longo A
        • Avitabile T
        • Bonfiglio V
        • Russo A
        • et al.
        Risk of acute stroke in patients with retinal artery occlusion: A systematic review and meta-analysis.
        Eye (Lond), 2019
        • Zhang LY
        • Zhang J
        • Kim RK
        • Matthews JL
        • Rudich DS
        • Greer DM
        • et al.
        Risk of acute ischemic stroke in patients with monocular vision loss of vascular etiology.
        J Neuroophthalmol. 2018; 38: 328-333
        • Lavin P
        • Patrylo M
        • Hollar M
        • Espaillat KB
        • Kirshner H
        • Schrag M.
        Stroke risk and risk factors in patients with central retinal artery occlusion.
        Am J Ophthalmol. 2018; 196: 96-100
        • Lauda F
        • Neugebauer H
        • Reiber L
        • Jüttler E.
        Acute silent brain infarction in monocular visual loss of ischemic origin.
        Cerebrovasc Dis. 2015; 40: 151-156
        • Margo CE
        • Mack WP.
        Therapeutic decisions involving disparate clinical outcomes: Patient preference survey for treatment of central retinal artery occlusion.
        Ophthalmology. 1996; 103: 691-696
        • Mac Grory B
        • Lavin P
        • Kirshner H
        • Schrag M
        Thrombolytic therapy for acute central retinal artery occlusion.
        Stroke. 2020; 51: 687-695
        • Dumitrascu OM
        • Newman NJ
        • Biousse V.
        Thrombolysis for central retinal artery occlusion in 2020: Time is vision!.
        J Neuroophthalmol. 2020;
        • McLeod D
        • Beatty S.
        Evidence for an enduring ischaemic penumbra following central retinal artery occlusion, with implications for fibrinolytic therapy.
        Prog Retin Eye Res. 2015; 49: 82-119
        • Hayreh SS
        • Weingeist TA.
        Experimental occlusion of the central artery of the retina. Iv: Retinal tolerance time to acute ischaemia.
        Br J Ophthalmol. 1980; 64: 818-825
        • Hayreh SS
        • Weingeist TA.
        Experimental occlusion of the central artery of the retina. I. Ophthalmoscopic and fluorescein fundus angiographic studies.
        Br J Ophthalmol. 1980; 64: 896-912
        • Hayreh SS
        • Jonas JB.
        Optic disk and retinal nerve fiber layer damage after transient central retinal artery occlusion: An experimental study in rhesus monkeys.
        Am J Ophthalmol. 2000; 129: 786-795
        • Hayreh SS
        • Zimmerman MB
        • Kimura A
        • Sanon A.
        Central retinal artery occlusion. Retinal survival time.
        Exp Eye Res. 2004; 78: 723-736
      1. Tissue plasminogen activator for acute ischemic stroke. The national institute of neurological disorders and stroke rt-pa stroke study group.
        N Engl J Med. 1995; 333: 1581-1587
        • Hacke W
        • Kaste M
        • Bluhmki E
        • Brozman M
        • Dávalos A
        • Guidetti D
        • et al.
        Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke.
        N Engl J Med. 2008; 359: 1317-1329
        • Lees KR
        • Bluhmki E
        • von Kummer R
        • Brott TG
        • Toni D
        • Grotta JC
        • et al.
        Time to Treatment with Intravenous Alteplase and Outcome in Stroke: An Updated Pooled Analysis of Ecass, Atlantis, Ninds, and Epithet Trials. 375. Lancet (London, England, 2010: 1695-1703
        • Thomalla G
        • Cheng B
        • Ebinger M
        • Hao Q
        • Tourdias T
        • Wu O
        • et al.
        Dwi-flair mismatch for the identification of patients with acute ischaemic stroke within 4·5 h of symptom onset (pre-flair): a multicentre observational study.
        The Lancet Neurol. 2011; 10: 978-986
        • Schwamm LH
        • Wu O
        • Song SS
        • Latour LL
        • Ford AL
        • Hsia AW
        • et al.
        Intravenous thrombolysis in unwitnessed stroke onset: Mr witness trial results.
        Ann Neurol. 2018; 83: 980-993
        • Thomalla G
        • Simonsen CZ
        • Boutitie F
        • Andersen G
        • Berthezene Y
        • Cheng B
        • et al.
        MRI-guided thrombolysis for stroke with unknown time of onset.
        N Engl J Med. 2018; 379: 611-622
        • Ma H
        • Campbell BCV
        • Parsons MW
        • Churilov L
        • Levi CR
        • Hsu C
        • et al.
        Thrombolysis guided by perfusion imaging up to 9 hours after onset of stroke.
        N Engl J Med. 2019; 380: 1795-1803
        • Berkhemer OA
        • Fransen PS
        • Beumer D
        • van den Berg LA
        • Lingsma HF
        • Yoo AJ
        • et al.
        A randomized trial of intraarterial treatment for acute ischemic stroke.
        N Engl J Med. 2015; 372: 11-20
        • Goyal M
        • Demchuk AM
        • Menon BK
        • Eesa M
        • Rempel JL
        • Thornton J
        • et al.
        Randomized assessment of rapid endovascular treatment of ischemic stroke.
        N Engl J Med. 2015; 372: 1019-1030
        • Campbell BC
        • Mitchell PJ
        • Kleinig TJ
        • Dewey HM
        • Churilov L
        • Yassi N
        • et al.
        Endovascular therapy for ischemic stroke with perfusion-imaging selection.
        N Engl J Med. 2015; 372: 1009-1018
        • Saver JL
        • Goyal M
        • Bonafe A
        • Diener HC
        • Levy EI
        • Pereira VM
        • et al.
        Stent-retriever thrombectomy after intravenous t-pa vs. T-pa alone in stroke.
        N Engl J Med. 2015; 372: 2285-2295
        • Jovin TG
        • Chamorro A
        • Cobo E
        • de Miquel MA
        • Molina CA
        • Rovira A
        • et al.
        Thrombectomy within 8 hours after symptom onset in ischemic stroke.
        N Engl J Med. 2015; 372: 2296-2306
        • Goyal M
        • Menon BK
        • van Zwam WH
        • Dippel DW
        • Mitchell PJ
        • Demchuk AM
        • et al.
        Endovascular thrombectomy after large-vessel ischaemic stroke: a meta-analysis of individual patient data from five randomised trials.
        Lancet. 2016; 387: 1723-1731
        • Wheeler HM
        • Mlynash M
        • Inoue M
        • Tipirnini A
        • Liggins J
        • Bammer R
        • et al.
        The growth rate of early dwi lesions is highly variable and associated with penumbral salvage and clinical outcomes following endovascular reperfusion.
        Int J Stroke. 2015; 10: 723-729
        • Albers GW.
        Late window paradox.
        Stroke. 2018; 49: 768-771
        • Ma H
        • Campbell BCV
        • Parsons MW
        • Churilov L
        • Levi CR
        • Hsu C
        • et al.
        Thrombolysis guided by perfusion imaging up to 9 hours after onset of stroke.
        N Engl J Med. 2019; 380: 1795-1803
        • Brown GC
        • Shields JA.
        Cilioretinal arteries and retinal arterial occlusion.
        Arch Ophthalmol. 1979; 97: 84-92
        • Biousse V
        • Newman NJ.
        Ischemic optic neuropathies.
        N Engl J Med. 2015; 372: 2428-2436
        • Tobalem S
        • Schutz JS
        • Chronopoulos A.
        Central retinal artery occlusion - rethinking retinal survival time.
        BMC Ophthalmol. 2018; 18: 101
        • Landers MB.
        Retinal oxygenation via the choroidal circulation.
        Trans Am Ophthalmol Soc. 1978; 76: 528-556
        • Wangsa-Wirawan ND
        • Linsenmeier RA.
        Retinal oxygen: fundamental and clinical aspects.
        Arch Ophthalmol. 2003; 121: 547-557
        • Dollery CT
        • Bulpitt CJ
        • Kohner EM.
        Oxygen supply to the retina from the retinal and choroidal circulations at normal and increased arterial oxygen tensions.
        Invest Ophthalmol. 1969; 8: 588-594
        • Hayreh SS.
        Blood supply of the optic nerve head and its role in optic atrophy, glaucoma, and oedema of the optic disc.
        Br J Ophthalmol. 1969; 53: 721-748
        • Kim YS
        • Nam MS
        • Park EJ
        • Lee Y
        • Kim H
        • Kim SH
        • et al.
        The effect of adjunctive hyperbaric oxygen therapy in patients with central retinal artery occlusion.
        Undersea Hyperb Med. 2020; 47: 57-64
        • Ferreira D
        • Soares C
        • Tavares-Ferreira J
        • Fernandes T
        • Araújo R
        • Castro P.
        Acute phase treatment in central retinal artery occlusion: thrombolysis, hyperbaric oxygen therapy or both?.
        J Thromb Thromb. 2020;
        • Masters TC
        • Westgard BC
        • Hendriksen SM
        • Decanini A
        • Abel AS
        • Logue CJ
        • et al.
        Case series of hyperbaric oxygen therapy for central retinal artery occlusion.
        Retin Cases Brief Rep. 2019;
        • Wu X
        • Chen S
        • Li S
        • Zhang J
        • Luan D
        • Zhao S
        • et al.
        Oxygen therapy in patients with retinal artery occlusion: A meta-analysis.
        PLoS One. 2018; 13 (e0202154)
        • Mac Grory B
        • Schrag M
        • Biousse V
        • Furie KL
        • Gerhard-Herman M
        • Lavin PJ
        • et al.
        Management of central retinal artery occlusion: a scientific statement from the american heart association.
        Stroke. 2021; (STR0000000000000366)
        • Vestergaard N
        • Cehofski LJ
        • Honoré B
        • Aasbjerg K
        • Vorum H.
        Animal models used to simulate retinal artery occlusion: a comprehensive review.
        Transl Vis Sci Technol. 2019; 8: 23
        • Hayreh SS
        • Zimmerman MB.
        Fundus changes in central retinal artery occlusion.
        Retina. 2007; 27: 276-289
        • Brancato R
        • Trabucchi G.
        Fluorescein and indocyanine green angiography in vascular chorioretinal diseases.
        Semin Ophthalmol. 1998; 13: 189-198
        • Yannuzzi LA
        • Rohrer KT
        • Tindel LJ
        • Sobel RS
        • Costanza MA
        • Shields W
        • et al.
        Fluorescein angiography complication survey.
        Ophthalmology. 1986; 93: 611-617
        • Hope-Ross M
        • Yannuzzi LA
        • Gragoudas ES
        • Guyer DR
        • Slakter JS
        • Sorenson JA
        • et al.
        Adverse reactions due to indocyanine green.
        Ophthalmology. 1994; 101: 529-533
        • Kwiterovich KA
        • Maguire MG
        • Murphy RP
        • Schachat AP
        • Bressler NM
        • Bressler SB
        • et al.
        Frequency of adverse systemic reactions after fluorescein angiography. results of a prospective study.
        Ophthalmology. 1991; : 1139-1142
        • Hayreh SS.
        Prevalent misconceptions about acute retinal vascular occlusive disorders.
        Prog Retin Eye Res. 2005; 24: 493-519
        • Mendis KR
        • Balaratnasingam C
        • Yu P
        • Barry CJ
        • McAllister IL
        • Cringle SJ
        • et al.
        Correlation of histologic and clinical images to determine the diagnostic value of fluorescein angiography for studying retinal capillary detail.
        Invest Ophthalmol Vis Sci. 2010; 51: 5864-5869
        • Rudkin AK
        • Lee AW
        • Chen CS.
        Ocular neovascularization following central retinal artery occlusion: prevalence and timing of onset.
        Eur J Ophthalmol. 2010; 20: 1042-1046
        • Coleman DJ
        • Silverman RH
        • Rondeau MJ
        • Lloyd HO
        • Daly S.
        Explaining the current role of high frequency ultrasound in ophthalmic diagnosis (ophthalmic ultrasound).
        Expert Rev Ophthalmol. 2006; 1: 63-76
      2. Fda guidance for industry and fda staff. Information for manufacturers seeking marketing clearance of diagnostic ultrasound systems and transducers, september 9, 2008. https://www.Fda.Gov/downloads/ucm070911.Pdf. accessed february 25, 2019.

        • Fielding JA.
        The assessment of ocular injury by ultrasound.
        Clin Radiol. 2004; 59: 301-312
        • Kim HH
        • Cannata JM
        • Liu R
        • Chang JH
        • Silverman RH
        • Shung KK.
        20 mhz/40 mhz dual element transducers for high frequency harmonic imaging.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2008; 55: 2683-2691
        • Dennis KJ
        • Dixon RD
        • Winsberg F
        • Ernest JT
        • Goldstick TK.
        Variability in measurement of central retinal artery velocity using color doppler imaging.
        J Ultrasound Med. 1995; 14: 463-466
        • Dimitrova G
        • Kato S.
        Color doppler imaging of retinal diseases.
        Surv Ophthalmol. 2010; 55: 193-214
        • Montaldo G
        • Tanter M
        • Bercoff J
        • Benech N
        • Fink M.
        Coherent plane-wave compounding for very high frame rate ultrasonography and transient elastography.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2009; 56: 489-506
        • Macé E
        • Montaldo G
        • Cohen I
        • Baulac M
        • Fink M
        • Tanter M.
        Functional ultrasound imaging of the brain.
        Nat Methods. 2011; 8: 662-664
        • Bercoff J
        • Montaldo G
        • Loupas T
        • Savery D
        • Mézière F
        • Fink M
        • et al.
        Ultrafast compound doppler imaging: providing full blood flow characterization.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2011; 58: 134-147
        • Urs R
        • Ketterling JA
        • Silverman RH.
        Ultrafast ultrasound imaging of ocular anatomy and blood flow.
        Invest Ophthalmol Vis Sci. 2016; 57: 3810-3816
        • Urs R
        • Ketterling JA
        • Yu ACH
        • Lloyd HO
        • Yiu BYS
        • Silverman RH.
        Ultrasound imaging and measurement of choroidal blood flow.
        Transl Vis Sci Technol. 2018; 7: 5
        • Christensen-Jeffries K
        • Browning RJ
        • Tang MX
        • Dunsby C
        • Eckersley RJ.
        In vivo acoustic super-resolution and super-resolved velocity mapping using microbubbles.
        IEEE Trans Med Imaging. 2015; 34: 433-440
        • Errico C
        • Pierre J
        • Pezet S
        • Desailly Y
        • Lenkei Z
        • Couture O
        • et al.
        Ultrafast ultrasound localization microscopy for deep super-resolution vascular imaging.
        Nature. 2015; 527: 499-502
        • Qian X
        • Kang H
        • Li R
        • Lu G
        • Du Z
        • Shung KK
        • et al.
        In vivo visualization of eye vasculature using super-resolution ultrasound microvessel imaging.
        IEEE Trans Biomed Eng. 2020;
        • Urs R
        • Ketterling JA
        • Tezel G
        • Silverman RH.
        Contrast-enhanced plane-wave ultrasound imaging of the rat eye.
        Exp Eye Res. 2020; 193107986
        • Kaiser HJ
        • Schötzau A
        • Flammer J.
        Blood-flow velocities in the extraocular vessels in normal volunteers.
        Am J Ophthalmol. 1996; 122: 364-370
        • Ertl M
        • Altmann M
        • Torka E
        • Helbig H
        • Bogdahn U
        • Gamulescu A
        • et al.
        The retrobulbar "Spot sign" As a discriminator between vasculitic and thrombo-embolic affections of the retinal blood supply.
        Ultraschall Med. 2012; 33 (E263-e267)
        • Foroozan R
        • Savino PJ
        • Sergott RC.
        Embolic central retinal artery occlusion detected by orbital color doppler imaging.
        Ophthalmology. 2002; 109 (discussion 747-748): 744-747
        • Nedelmann M
        • Graef M
        • Weinand F
        • Wassill KH
        • Kaps M
        • Lorenz B
        • et al.
        Retrobulbar spot sign predicts thrombolytic treatment effects and etiology in central retinal artery occlusion.
        Stroke. 2015; 46: 2322-2324
        • Altmann M
        • Ertl M
        • Helbig H
        • Schömig B
        • Bogdahn U
        • Gamulescu MA
        • et al.
        Low endogenous recanalization in embolic central retinal artery occlusion-the retrobulbar "Spot sign".
        J Neuroimaging. 2015; 25: 251-256
        • Nedelmann M
        • Tanislav C
        • traveling Kaps M.A
        Spot sign" In recurrent amaurosis fugax and central retinal artery occlusion.
        J Stroke Cerebrovasc Dis. 2014; 23: e421-e422
        • Coleman DJ.
        Reliability of ocular and orbital diagnosis with b-scan ultrasound. 1. ocular diagnosis.
        Am J Ophthalmol. 1972; 73: 501-516
        • Lopez D
        • Guevara M.
        Use of ultrasound in the diagnosis and management of the vasculitides.
        Curr Rheumatol Rep. 2020; 22: 31
        • Nesher G
        • Shemesh D
        • Mates M
        • Sonnenblick M
        • Abramowitz HB.
        The predictive value of the halo sign in color doppler ultrasonography of the temporal arteries for diagnosing giant cell arteritis.
        J Rheumatol. 2002; 29: 1224-1226
        • Huang D
        • Swanson EA
        • Lin CP
        • Schuman JS
        • Stinson WG
        • Chang W
        • et al.
        Optical coherence tomography.
        Science. 1991; 254: 1178-1181
        • Ferrara D
        • Mohler KJ
        • Waheed N
        • Adhi M
        • Liu JJ
        • Grulkowski I
        • et al.
        En face enhanced-depth swept-source optical coherence tomography features of chronic central serous chorioretinopathy.
        Ophthalmology. 2014; 121: 719-726
        • Chu YK
        • Hong YT
        • Byeon SH
        • Kwon OW.
        In vivo detection of acute ischemic damages in retinal arterial occlusion with optical coherence tomography: A "Prominent middle limiting membrane sign".
        Retina. 2013; 33: 2110-2117
        • Ahn SJ
        • Woo SJ
        • Park KH
        • Jung C
        • Hong JH
        • Han MK.
        Retinal and choroidal changes and visual outcome in central retinal artery occlusion: An optical coherence tomography study.
        Am J Ophthalmol. 2015; 159: 667-676
        • Matthe E
        • Eulitz P
        • Furashova O.
        Acute retinal ischemia in central versus branch retinal artery occlusion: Changes in retinal layers' thickness on spectral-domain optical coherence tomography in different grades of retinal ischemia.
        Retina. 2020; 40: 1118-1123
        • Chen H
        • Xia H
        • Qiu Z
        • Chen W
        • Chen X.
        Correlation of optical intensity on optical coherence tomography and visual outcome in central retinal artery occlusion.
        Retina. 2016; 36: 1964-1970
        • Ochakovski GA
        • Wenzel DA
        • Spitzer MS
        • Poli S
        • Härtig F
        • Fischer MD
        • et al.
        Retinal oedema in central retinal artery occlusion develops as a function of time.
        Acta Ophthalmol. 2020;
        • Wenzel DA
        • Kromer R
        • Poli S
        • Steinhorst NA
        • Casagrande MK
        • Spitzer MS
        • et al.
        Optical coherence tomography-based determination of ischaemia onset - the temporal dynamics of retinal thickness increase in acute central retinal artery occlusion.
        Acta Ophthalmol. 2020;
        • Schultheiss M
        • Hartig F
        • Spitzer MS
        • Feltgen N
        • Spitzer B
        • Husing J
        • et al.
        Intravenous thrombolysis in acute central retinal artery occlusion - a prospective interventional case series.
        PLoS One. 2018; 13 (e0198114)
        • Furashova O
        • Matthe E.
        Retinal changes in different grades of retinal artery occlusion: an optical coherence tomography study.
        Invest Ophthalmol Vis Sci. 2017; 58: 5209-5216
        • Wang RK
        • Jacques SL
        • Ma Z
        • Hurst S
        • Hanson SR
        • Gruber A.
        Three dimensional optical angiography.
        Opt Express. 2007; 15: 4083-4097
        • Bonini Filho MA
        • Adhi M
        • de Carlo TE
        • Ferrara D
        • Baumal CR
        • Witkin AJ
        • et al.
        Optical coherence tomography angiography in retinal artery occlusion.
        Retina. 2015; 35: 2339-2346
        • Baumal CR.
        Optical coherence tomography angiography of retinal artery occlusion.
        Dev Ophthalmol. 2016; 56: 122-131
        • Yang S
        • Liu X
        • Li H
        • Xu J
        • Wang F.
        Optical coherence tomography angiography characteristics of acute retinal arterial occlusion.
        BMC Ophthalmol. 2019; 19: 147
        • Konno A
        • Ishibazawa A
        • Ro-Mase T
        • Ishiko S
        • Song YS
        • Nishikawa N
        • et al.
        Circumpapillary collateral vessel development in iatrogenic central retinal artery occlusion observed using oct angiography.
        Am J Ophthalmol Case Rep. 2020; 19100740
        • Ghashut R
        • Muraoka Y
        • Ooto S
        • Iida Y
        • Miwa Y
        • Suzuma K
        • et al.
        Evaluation of macular ischemia in eyes with central retinal vein occlusion: an optical coherence tomography angiography study.
        Retina. 2018; 38: 1571-1580
        • Gao SS
        • Jia Y
        • Zhang M
        • Su JP
        • Liu G
        • Hwang TS
        • et al.
        Optical coherence tomography angiography.
        Invest Ophthalmol Vis Sci. 2016; 57 (OCT27-36)
        • De Oliveira PR
        • Berger AR
        • Chow DR.
        Optical coherence tomography angiography in chorioretinal disorders.
        Can J Ophthalmol. 2017; 52: 125-136
        • Nelson DA
        • Krupsky S
        • Pollack A
        • Aloni E
        • Belkin M
        • Vanzetta I
        • et al.
        Special report: Noninvasive multi-parameter functional optical imaging of the eye.
        Ophthalmic Surg Lasers Imaging. 2005; 36: 57-66
        • Delori FC.
        Noninvasive technique for oximetry of blood in retinal vessels.
        Appl Opt. 1988; 27: 1113-1125
        • Chhablani J
        • Bartsch DU
        • Cheng L
        • Gomez L
        • Alshareef RA
        • Rezeq SS
        • et al.
        Segmental reproducibility of retinal blood flow velocity measurements using retinal function imager.
        Graefes Arch Clin Exp Ophthalmol. 2013; 251: 2665-2670
        • Burgansky-Eliash Z
        • Nelson DA
        • Bar-Tal OP
        • Lowenstein A
        • Grinvald A
        • Barak A.
        Reduced retinal blood flow velocity in diabetic retinopathy.
        Retina. 2010; 30: 765-773
        • Jiang H
        • Delgado S
        • Tan J
        • Liu C
        • Rammohan KW
        • DeBuc DC
        • et al.
        Impaired retinal microcirculation in multiple sclerosis.
        Mult Scler. 2016; 22: 1812-1820
        • Beutelspacher SC
        • Serbecic N
        • Barash H
        • Burgansky-Eliash Z
        • Grinvald A
        • Krastel H
        • et al.
        Retinal blood flow velocity measured by retinal function imaging in retinitis pigmentosa.
        Graefes Arch Clin Exp Ophthalmol. 2011; 249: 1855-1858
        • Jittpoonkuson T
        • Garcia P
        • Landa G
        • Rosen R.
        Retinal blood-flow velocity and oximetry status monitoring in a central retinal vein occlusion patient.
        . 2009; 6: 52-54
        • Kim J
        • Lee D
        • Jung U
        • Kim C.
        Photoacoustic imaging platforms for multimodal imaging.
        Ultrasonography. 2015; 34: 88-97
        • Harris A
        • Dinn RB
        • Kagemann L
        • Rechtman E.
        A review of methods for human retinal oximetry.
        Ophthalmic Surg Lasers Imaging. 2003; 34: 152-164
        • Song W
        • Wei Q
        • Liu W
        • Liu T
        • Yi J
        • Sheibani N
        • et al.
        A combined method to quantify the retinal metabolic rate of oxygen using photoacoustic ophthalmoscopy and optical coherence tomography.
        Sci Rep. 2014; 4: 6525
        • Liu X
        • Liu T
        • Wen R
        • Li Y
        • Puliafito CA
        • Zhang HF
        • et al.
        Optical coherence photoacoustic microscopy for in vivo multimodal retinal imaging.
        Opt Lett. 2015; 40: 1370-1373
        • Tian C
        • Zhang W
        • Mordovanakis A
        • Wang X
        • Paulus YM.
        Noninvasive chorioretinal imaging in living rabbits using integrated photoacoustic microscopy and optical coherence tomography.
        Opt Express. 2017; 25: 15947-15955
        • Hariri A
        • Wang J
        • Kim Y
        • Jhunjhunwala A
        • Chao DL
        • Jokerst JV.
        In vivo photoacoustic imaging of chorioretinal oxygen gradients.
        J Biomed Opt. 2018; 23: 1-8
        • Briers D
        • Duncan DD
        • Hirst E
        • Kirkpatrick SJ
        • Larsson M
        • Steenbergen W
        • et al.
        Laser speckle contrast imaging: Theoretical and practical limitations.
        J Biomed Opt. 2013; 18066018
        • Hoover EM
        • Crouzet C
        • Bordas JM
        • Figueroa Velez DX
        • Gandhi SP
        • Choi B
        • et al.
        Transcranial chronic optical access to longitudinally measure cerebral blood flow.
        J Neurosci Methods. 2020; 350109044
        • Dunn AK.
        Laser speckle contrast imaging of cerebral blood flow.
        Ann Biomed Eng. 2012; 40: 367-377
        • Briers JD
        • Fercher AF.
        Retinal blood-flow visualization by means of laser speckle photography.
        Invest Ophthalmol Vis Sci. 1982; 22: 255-259
        • Neganova AY
        • Postnov DD
        • Jacobsen JC
        • Sosnovtseva O.
        Laser speckle analysis of retinal vascular dynamics.
        Biomed Opt Express. 2016; 7: 1375-1384
        • Takata Y
        • Nitta Y
        • Miyakoshi A
        • Hayashi A.
        Retinal endovascular surgery with tissue plasminogen activator injection for central retinal artery occlusion.
        Case Rep Ophthalmol. 2018; 9: 327-332
        • Patel DD
        • Lipinski DM.
        Validating a low-cost laser speckle contrast imaging system as a quantitative tool for assessing retinal vascular function.
        Sci Rep. 2020; 10: 7177
        • Jiao S
        • Jiang M
        • Hu J
        • Fawzi A
        • Zhou Q
        • Shung KK
        • et al.
        Photoacoustic ophthalmoscopy for in vivo retinal imaging.
        Opt Express. 2010; 18: 3967-3972

      Linked Article

      • Response by Mac Grory et al. to Letter regarding “Structural and Functional Imaging of the Retina in Central Retinal Artery Occlusion – Current Approaches and Future Directions”
        Journal of Stroke and Cerebrovascular DiseasesVol. 30Issue 10
        • Preview
          We wish to thank Drs. Tuuminen, Achiron and Kanclerz for the interest in our paper and for the opportunity to address several entrenched misconceptions about the treatment of central retinal artery occlusion (CRAO). In 2015, Schrag et al.1 published a subject level meta-analysis concerning visual outcomes in patients with CRAO who were untreated, treated with thrombolysis or treated with a variety of conservative therapies (anterior chamber paracentesis, ocular massage and/or hemodilution). An important innovation in this work was the use of a simple, reproducible definition of visual recovery as the attainment of a final visual acuity of ≥20/100 in the affected eye.
        • Full-Text
        • PDF
      • Controversies on the Recommended Treatment for Central Retinal Artery Occlusion
        Journal of Stroke and Cerebrovascular DiseasesVol. 30Issue 10
        • Preview
          In a recent article, Mac Grory et al.1 described the structural and functional retinal imaging modalities in central retinal artery occlusion (CRAO). They have also suggested that thrombolysis is emerging as a compelling therapeutic approach for CRAO treatment, and should be administered shortly after the onset of visual loss to induce recanalisation of the occluded retinal arteries and reperfusion of the ischemic retina before retinal cell death. Importantly, there is considerable variability in CRAO management patterns among practitioners, institutions, and subspecialty groups.
        • Full-Text
        • PDF