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Fundus autofluorescence in retinal artery occlusion: A more precise diagnosis
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Fundus autofluorescence in retinal artery occlusion: A more precise diagnosis Intérêt de l’autofluorescence dans l’évaluation des emboles artériels rétiniens J.-L. Bacquet a, M. Sarov-Rivière b, C. Denier b, G. Querques c, B. Riou a, L. Bonin a, E. Barreau a, M. Labetoulle a, A. Rousseau a,∗ a
Service d’ophtalmologie, hôpital Bicêtre, université Paris-Sud, DHU vision et handicaps, Assistance publique—Hôpitaux de Paris, 78, rue du Général-Leclerc, 94275 Le Kremlin-Bicêtre cedex, France b Service de neurologie, hôpital Bicêtre, université Paris-Sud, Assistance publique—Hôpitaux de Paris, 78, rue du Général-Leclerc, 94275 Le Kremlin-Bicêtre, France c Service d’ophtalmologie, centre hospitalier intercommunal de Créteil, université Paris-Est, DHU vision et handicaps, 78, rue du Général-Leclerc, 94275 Le Kremlin-Bicêtre cedex, France Received 6 December 2016; accepted 9 March 2017
KEYWORDS Emboli; Retinal artery occlusion; Fundus autofluorescence; Lipofuscin; Plaque
∗
Summary Importance. — Retinal artery occlusion (RAO) is a medical emergency associated with a high risk of cerebral vascular accident and other cardiovascular events. Among patients with nonarteritic RAO, a retinal embolus is observed in approximately 40% of cases. Fundus examination and retinography are not reliable to predict the nature of the emboli. Observations. — We report three consecutive cases of central and branch RAO that were investigated with fundus autofluorescence, fluorescein angiography and color retinal photographs. All patients underwent complete neurological and cardiovascular workups, with brain imaging, cardiac Doppler ultrasound, carotid Dopplers and Holter ECG’s, to determine the underlying mechanism of retinal embolism. In the three cases, aged 77.7 ± 4 years (2 women and 1 man), fundus autofluorescence demonstrated hyperautofluorescent emboli. In two cases, it allowed visualization of emboli that were not detected with fundus examination or retinography. The cardiovascular work-up demonstrated atheromatous carotid or aortic plaques in all patients. In one case, it permitted the diagnosis of RAO. Two of the three cases were considered to be of atherosclerotic origin and one of undefined origin.
Corresponding author. E-mail address: [email protected] (A. Rousseau).
http://dx.doi.org/10.1016/j.jfo.2017.03.010 0181-5512/© 2017 Elsevier Masson SAS. All rights reserved.
Please cite this article in press as: Bacquet J-L, et al. Fundus autofluorescence in retinal artery occlusion: A more precise diagnosis. J Fr Ophtalmol (2017), http://dx.doi.org/10.1016/j.jfo.2017.03.010
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J.-L. Bacquet et al. Conclusion and relevance. — Fundus autofluorescence may help to detect and characterize retinal emboli. Since lipofuscin, which is present in large quantity in atherosclerotic plaques, is the main fluorophore detected with fundus autofluorescence, this non-invasive and simple examination may give information about the underlying mechanism of retinal embolism, and thus impact the etiologic assessment of RAO. Additional studies are necessary to confirm this potential role of autofluorescence. © 2017 Elsevier Masson SAS. All rights reserved.
MOTS CLÉS Emboles ; Occlusion artérielle ; Autofluorescence ; Lipofuscine ; Athérome
Résumé Introduction. — Les occlusions artérielles rétiniennes (OAR) constituent des équivalents rétiniens d’accident vasculaire cérébral (AVC). Les emboles artériels rétiniens ne sont pas toujours visibles au fond d’œil et leur aspect ne permet pas de préjuger de leur nature. Observations. — Nous rapportons 3 cas consécutifs d’OAR ayant bénéficié d’un examen ophtalmologique complet avec cliché en autofluorescence, angiographie à la fluorescéine et rétinographie couleur. Ils bénéficiaient de plus d’un bilan cardiovasculaire et neurologique avec imagerie cérébrale, échographie-Doppler cardiaque et des troncs supra-aortiques et holter ECG. Les 3 patients âgés de 77,7 ± 4 ans (2 femmes et un homme) présentaient des emboles artériels hyper autofluorescents dont deux n’avaient pas été détectés au fond d’œil. Le bilan cardiovasculaire mettait en évidence des plaques athéromateuses carotidiennes ou aortiques chez tous les patients. Chez 2 patients, le diagnostic d’AVC rétinien d’origine athéromateuse était retenu. Chez la 3e patiente, le diagnostic étiologique ne pouvait être retenu avec certitude. Conclusion. — Au niveau rétinien, l’hyper-autofluorescence est habituellement associée à la présence de lipofuscine, qui est également présente en grande quantité dans les plaques athéromateuses. L’autofluorescence pourrait faciliter la détection des emboles rétiniens. Des études supplémentaires sont nécessaires pour affirmer l’intérêt de l’autofluorescence pour établir la nature des emboles rétiniens. © 2017 Elsevier Masson SAS. Tous droits r´ eserv´ es.
Introduction Retinal artery occlusion (RAO) is a medical emergency associated with a high risk of cerebral vascular accident and other cardiovascular events [1,2]. Among patients with nonarteritic RAO, a retinal embolus is observed in approximately 40% of case and can be of different nature, depending on the underlying mechanism [3]. Fibrinocruoric emboli may occur in embolic heart disease such as auricular fibrillation; calcic emboli usually originate from a calcified aortic valve and atherosclerotic emboli usually originate from an atheromatous plaque within the carotid arteries or the aorta [4,5]. Other types of emboli (tumoral, fatty) are much less frequent. Each type of embolism implies specific management and therefore, diagnosing the origin of arterial retinal emboli is of crucial importance. Unfortunately, funduscopic examination and retinography are not reliable to determine the nature of the emboli [6]. Fundus autofluorescence imaging is a non invasive imaging method that allows visualization of lipofuscin in the retina as well as of other fluorophores that may occur with retinal diseases [7]. We herein report a case series of 3 patients with RAO in which fundus autoflorescence contributed to the diagnosis and/or the management. We discuss the interest of this particular finding, its
suspected underlying mechanisms, and how it may impact RAO assessment.
Case 1 A 77-year-old woman with multiple cardiovascular risk factors was referred for a sudden loss of vision of the left eye. The visual acuity was 20/200 OS. Slit lamp examination was normal except for a grade 2 corticonuclear cataract. The fundus examination revealed an inferior macular ischemic edema and 2 arteriolar retinal emboli along the inferotemporal arcade (Fig. 1A). She underwent a complete cardiovascular work-up, which revealed extensive aortic atherosclerotic plaques and a severe right carotid stenosis (Table 1). The 24-hour electrocardiogram and the echocardiogram were negative for cardiac cause of embolism. Laboratory investigations revealed a normal erythrocyte sedimentation rate and C-reactive protein, and a hypercholesterolemia. This retinal stroke was considered to be due to an atherosclerotic origin. After 15 days, she came back to perform a fluorescein angiography. Fundus autofluorescence revealed 3 hyperautofluorescent dots corresponding to the arteriolar emboli (Fig. 1C). A third embolus on the central retinal artery trunk, which had been overlooked on
Please cite this article in press as: Bacquet J-L, et al. Fundus autofluorescence in retinal artery occlusion: A more precise diagnosis. J Fr Ophtalmol (2017), http://dx.doi.org/10.1016/j.jfo.2017.03.010
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Figure 1. Case 1. A. Retinography of the left eye showing 2 arteriolar emboli along the inferotemporal arcade (arrowheads) and ischemic edema of the retina. B. Retinography 15 days after: barely visible embolus at the level of the trunk of the central retinal artery. C. Fundus autofluorescence: hypoautofluorescence of the ischemic zone and hyperautofluorescence of the retinal emboli. D. Fluorescein angiogram at the early phase: extensive non perfusion area.
the retinography (Fig. 1B), had appeared in the interval. This new embolic event led to reinforce the antiplatelet therapy. Fluorescein angiogram showed extensive area of non-perfusion (Fig. 1D), which was later treated by retinal panphotocoagulation.
cardiovascular work-up disclosed calcific aortic valve disease (Table 1). The pacemaker interrogation was positive for multiple atrial fibrillation episodes. Emboli could result either from aortic calcic emboli or from arrhythmia. Therefore, the cause of the retinal stroke could not be defined.
Case 2
Case 3
An 82-year-old woman was referred for a sudden loss of vision of the right eye. Her past history was positive for type 2 diabetes, hypertriglyceridemia and sinus node dysfunction treated with a pacemaker. She had a past history of bilateral macular degeneration. Fundus examination was blurry due to a dense cataract. However, It revealed macular exudates (Fig. 2A). There was no sign exudation on the macular OCT. Fundus autofluorescence showed a sharp hyperautofluorescence at the level of the superior hemitrunk of the central retinal artery (Fig. 2B). When examining carefully the retinography, this hyperautofluorescent zone matched with an arteriolar plaque (Fig. 2A, arrow), which was initially overlooked. Fluorescein angiogram revealed non-perfusion of the superotemporal retina, thus confirming the diagnosis of superior branch retinal artery occlusion. The
A 74-year-old pseudophakic man was referred for management of a central retinal artery occlusion of the right eye. The visual acuity was hand motion. He had a history of arterial hypertension, active tabagism (50 pack-years) and dyslipidemia. The fundus examination revealed a typical cherry-red spot within diffuse ischemic retinal edema, narrowed retinal arteries and a yellowish embolus at the level of the trunk of the retinal artery (Fig. 2C). Fundus autofluorescence showed macular hypoautofluorescence and revealed the embolus, which appeared as a sharp hyperautofluorescent spot (Fig. 2D). The cardiovascular work-up revealed a moderate right carotid stenosis (Table 1). The 24 h electrocardiogram and the echocardiogram were negative for cardiac cause of embolism. Brain MRI found a right thalamic infarction, however, neurologic examination was normal.
Please cite this article in press as: Bacquet J-L, et al. Fundus autofluorescence in retinal artery occlusion: A more precise diagnosis. J Fr Ophtalmol (2017), http://dx.doi.org/10.1016/j.jfo.2017.03.010
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J.-L. Bacquet et al. Table 1
Summary of clinical data, cardiovascular and neurologic workups.
Patient Age (years) Side of the Lens status retinal arterial occlusion
Cardiovascular Cardiovascular Neurologic risk factors workup workup
Presumed origin for the emboli
1
77
Left
Bilateral grade 2 corticonuclear cataract
Aortic and carotid atherosclerosis
2
82
Right
Bilateral grade 3 corticonuclear cataract
3
74
Right
Pseudophakic
Normal Severe right clinical carotid stenosis (ECST examination Brain CT 80%) Extensive angiography: aortic lacunar atheroscleinfarction of rotic plaques the right 24 h electrocaudate nucleus cardiogram: sinusal rhythm Echocardiogram: no intracardiac thrombus, normal ejection fraction Normal Treated hyper- Carotid clinical lipidemia plaques examination Hypertension without Normal brain Unbalanced stenosis type 2 Echocardiogram:CT severe calcific angiography diabetes (HbA1C: 7.9%) aortic valve stenosis Pacemaker interrogation: numerous atrial fibrillation episodes Right internal Normal Tobacco use clinical (50 PY) carotid Hyperlipidemia stenosis (ECST examination Brain MRI: left Hypertension 45%) Type 2 Extensive right thalamic infarction diabetes subclavian (HbA1C: 6%) plaques 24 h electrocardiogram: sinusal rhythm Echocardiogram: no intracardiac thrombus, normal ejection fraction Tobacco use (40 PY) Treated hyperlipidemia Hypertension
Not defined
Carotid atherosclerosis
PY: pack-year; ECST: European carotid surgery trial; CT: computed tomography; MRI: magnetic resonance imaging.
Please cite this article in press as: Bacquet J-L, et al. Fundus autofluorescence in retinal artery occlusion: A more precise diagnosis. J Fr Ophtalmol (2017), http://dx.doi.org/10.1016/j.jfo.2017.03.010
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Figure 2. A. Case 2. Retinography of the right eye. The fundus is blurred due to a dence corticonuclear cataract. An embolus is suspected at the level of the superior hemi-trunk of the central retinal artery (arrowhead). B. Case 2. Fundus autofluorescence: hyperautofluorescence of the embolus (arrowhead) and hypoautofluorescence of the ischemic macula. C. Case 3. Retinography of the right eye: typical cherry-red spot macula with visible embolus at the level of the trunk of the central retinal artery (arrowhead). D. Case 3. Fundus autofluorescence revealing the hyperautofluorescent embolus and the hypoautofluorescent ischemic retina.
Thus, this combined retinal and cerebral stroke was considered to be due to an atherosclerotic origin.
Discussion Funduscopic examination and retinography are not reliable to determine the nature of the emboli: both intra-observer and inter-observer agreement on the clinical qualitative assessment of retinal emboli is poor [6]. Moreover, fundus examination can be blurred by a dense cataract and altogether, retinal emboli are seen in less than half of the cases of retinal arterial occlusion [3]. Siddiqi et al. recently reported in a single clinical case that autofluorescence may highlight the retinal arterial emboli in RAO but did not discuss the underlying mechanism of autofluorescence of retinal emboli [8]. Moreover, autofluorescence shows hypofluorescence of the ischemic zones during the acute phase [9]. In the retina, the main fluorophore is lipofuscin, composed of lipid-containing residues of lysosomal digestion. Knowing that lipofuscin is found at high level in atherosclerotic plaques [10], it can be hypothesized that hyperautofluorescent emboli may originate from atherosclerotic plaques. However, Majstruk et al. recently
speculated that autofluorescence of retinal arterial plaques may be due to calcifications in the arterial wall [11]. In our series, 2 out of 3 patients with hyperautofluorescent emboli had evidence of an atherosclerotic origin of the vascular event. This case series confirms that fundus autofluorescence is a useful imaging technique for retinal artery occlusion and may help to detect arteriolar emboli. Although further studies, including patients with retinal emboli from various etiologies are warranted, fundus autofluorescence may help to define the nature of the retinal emboli, thus guiding the cardiovascular workup of this potentially lifethreatening disease.
Disclosure of interest The authors declare that they have no competing interest.
References [1] Biousse V. Acute retinal arterial ischemia: an emergency often ignored. Am J Ophthalmol 2014;157:1119—21.
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[2] Lee J, Kim SW, Lee SC, Kwon OW, Kim YD, Byeon SH. Cooccurrence of acute retinal artery occlusion and acute ischemic stroke: diffusion-weighted magnetic resonance imaging study. Am J Ophthalmol 2014;157:1231—8. [3] Sharma S, Brown GC, Cruess AF, Retinal emboli of cardiac origin study group. Accuracy of visible retinal emboli for the detection of cardioembolic lesions requiring anticoagulation or cardiac surgery. Br J Ophthalmol 1998;82:655—8. [4] Rousseau A, de Monchy I, Barreau E, Yahiaoui Y, M’Garrech M, Kaswin G, et al. Retinal emboli in cholesterol crystal embolism. Case Rep Ophthalmol Med 2013;2013:421352. [5] Taylor S, Lightman S. The eye in cardiac and cardiovascular disease. Hosp Med 2003;64:299—301. [6] Sharma S, Pater JL, Lam M, Cruess AF. Can different types of retinal emboli be reliably differentiated from one another? An inter- and intraobserver agreement study. Can J Ophthalmol 1998;33:144—8.
[7] Schmitz-Valckenberg S, Holz FG, Bird AC, Spaide RF. Fundus autofluorescence imaging: review and perspectives. Retina (Philadelphia, Pa) 2008;28:385—409. [8] Siddiqui AA, Paulus YM, Scott AW. Use of fundus autofluorescence to evaluate retinal artery occlusions. Retina (Philadelphia, Pa) 2014;34:2490—1. [9] Mathew R, Papavasileiou E, Sivaprasad S. Autofluorescence and high-definition optical coherence tomography of retinal artery occlusions. Clin Ophthalmol 2010;4:1159—63. [10] Tertov VV, Kaplun VV, Mikhailova IA, Suprun IV, Orekhov AN. The content of lipoperoxidation products in normal and atherosclerotic human aorta. Mol Cell Biochem 2001;225: 21—8. [11] Majstruk L, Giocanti-Auregan A. [Multimodal imaging of a Hollenhorst plaque]. J Fr Ophtalmol 2016;39:655—6.
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Journal français d’ophtalmologie (2017) xxx, xxx—xxx
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ORIGINAL ARTICLE
Fundus autofluorescence in retinal artery occlusion: A more precise diagnosis Intérêt de l’autofluorescence dans l’évaluation des emboles artériels rétiniens J.-L. Bacquet a, M. Sarov-Rivière b, C. Denier b, G. Querques c, B. Riou a, L. Bonin a, E. Barreau a, M. Labetoulle a, A. Rousseau a,∗ a
Service d’ophtalmologie, hôpital Bicêtre, université Paris-Sud, DHU vision et handicaps, Assistance publique—Hôpitaux de Paris, 78, rue du Général-Leclerc, 94275 Le Kremlin-Bicêtre cedex, France b Service de neurologie, hôpital Bicêtre, université Paris-Sud, Assistance publique—Hôpitaux de Paris, 78, rue du Général-Leclerc, 94275 Le Kremlin-Bicêtre, France c Service d’ophtalmologie, centre hospitalier intercommunal de Créteil, université Paris-Est, DHU vision et handicaps, 78, rue du Général-Leclerc, 94275 Le Kremlin-Bicêtre cedex, France Received 6 December 2016; accepted 9 March 2017
KEYWORDS Emboli; Retinal artery occlusion; Fundus autofluorescence; Lipofuscin; Plaque
∗
Summary Importance. — Retinal artery occlusion (RAO) is a medical emergency associated with a high risk of cerebral vascular accident and other cardiovascular events. Among patients with nonarteritic RAO, a retinal embolus is observed in approximately 40% of cases. Fundus examination and retinography are not reliable to predict the nature of the emboli. Observations. — We report three consecutive cases of central and branch RAO that were investigated with fundus autofluorescence, fluorescein angiography and color retinal photographs. All patients underwent complete neurological and cardiovascular workups, with brain imaging, cardiac Doppler ultrasound, carotid Dopplers and Holter ECG’s, to determine the underlying mechanism of retinal embolism. In the three cases, aged 77.7 ± 4 years (2 women and 1 man), fundus autofluorescence demonstrated hyperautofluorescent emboli. In two cases, it allowed visualization of emboli that were not detected with fundus examination or retinography. The cardiovascular work-up demonstrated atheromatous carotid or aortic plaques in all patients. In one case, it permitted the diagnosis of RAO. Two of the three cases were considered to be of atherosclerotic origin and one of undefined origin.
Corresponding author. E-mail address: [email protected] (A. Rousseau).
http://dx.doi.org/10.1016/j.jfo.2017.03.010 0181-5512/© 2017 Elsevier Masson SAS. All rights reserved.
Please cite this article in press as: Bacquet J-L, et al. Fundus autofluorescence in retinal artery occlusion: A more precise diagnosis. J Fr Ophtalmol (2017), http://dx.doi.org/10.1016/j.jfo.2017.03.010
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J.-L. Bacquet et al. Conclusion and relevance. — Fundus autofluorescence may help to detect and characterize retinal emboli. Since lipofuscin, which is present in large quantity in atherosclerotic plaques, is the main fluorophore detected with fundus autofluorescence, this non-invasive and simple examination may give information about the underlying mechanism of retinal embolism, and thus impact the etiologic assessment of RAO. Additional studies are necessary to confirm this potential role of autofluorescence. © 2017 Elsevier Masson SAS. All rights reserved.
MOTS CLÉS Emboles ; Occlusion artérielle ; Autofluorescence ; Lipofuscine ; Athérome
Résumé Introduction. — Les occlusions artérielles rétiniennes (OAR) constituent des équivalents rétiniens d’accident vasculaire cérébral (AVC). Les emboles artériels rétiniens ne sont pas toujours visibles au fond d’œil et leur aspect ne permet pas de préjuger de leur nature. Observations. — Nous rapportons 3 cas consécutifs d’OAR ayant bénéficié d’un examen ophtalmologique complet avec cliché en autofluorescence, angiographie à la fluorescéine et rétinographie couleur. Ils bénéficiaient de plus d’un bilan cardiovasculaire et neurologique avec imagerie cérébrale, échographie-Doppler cardiaque et des troncs supra-aortiques et holter ECG. Les 3 patients âgés de 77,7 ± 4 ans (2 femmes et un homme) présentaient des emboles artériels hyper autofluorescents dont deux n’avaient pas été détectés au fond d’œil. Le bilan cardiovasculaire mettait en évidence des plaques athéromateuses carotidiennes ou aortiques chez tous les patients. Chez 2 patients, le diagnostic d’AVC rétinien d’origine athéromateuse était retenu. Chez la 3e patiente, le diagnostic étiologique ne pouvait être retenu avec certitude. Conclusion. — Au niveau rétinien, l’hyper-autofluorescence est habituellement associée à la présence de lipofuscine, qui est également présente en grande quantité dans les plaques athéromateuses. L’autofluorescence pourrait faciliter la détection des emboles rétiniens. Des études supplémentaires sont nécessaires pour affirmer l’intérêt de l’autofluorescence pour établir la nature des emboles rétiniens. © 2017 Elsevier Masson SAS. Tous droits r´ eserv´ es.
Introduction Retinal artery occlusion (RAO) is a medical emergency associated with a high risk of cerebral vascular accident and other cardiovascular events [1,2]. Among patients with nonarteritic RAO, a retinal embolus is observed in approximately 40% of case and can be of different nature, depending on the underlying mechanism [3]. Fibrinocruoric emboli may occur in embolic heart disease such as auricular fibrillation; calcic emboli usually originate from a calcified aortic valve and atherosclerotic emboli usually originate from an atheromatous plaque within the carotid arteries or the aorta [4,5]. Other types of emboli (tumoral, fatty) are much less frequent. Each type of embolism implies specific management and therefore, diagnosing the origin of arterial retinal emboli is of crucial importance. Unfortunately, funduscopic examination and retinography are not reliable to determine the nature of the emboli [6]. Fundus autofluorescence imaging is a non invasive imaging method that allows visualization of lipofuscin in the retina as well as of other fluorophores that may occur with retinal diseases [7]. We herein report a case series of 3 patients with RAO in which fundus autoflorescence contributed to the diagnosis and/or the management. We discuss the interest of this particular finding, its
suspected underlying mechanisms, and how it may impact RAO assessment.
Case 1 A 77-year-old woman with multiple cardiovascular risk factors was referred for a sudden loss of vision of the left eye. The visual acuity was 20/200 OS. Slit lamp examination was normal except for a grade 2 corticonuclear cataract. The fundus examination revealed an inferior macular ischemic edema and 2 arteriolar retinal emboli along the inferotemporal arcade (Fig. 1A). She underwent a complete cardiovascular work-up, which revealed extensive aortic atherosclerotic plaques and a severe right carotid stenosis (Table 1). The 24-hour electrocardiogram and the echocardiogram were negative for cardiac cause of embolism. Laboratory investigations revealed a normal erythrocyte sedimentation rate and C-reactive protein, and a hypercholesterolemia. This retinal stroke was considered to be due to an atherosclerotic origin. After 15 days, she came back to perform a fluorescein angiography. Fundus autofluorescence revealed 3 hyperautofluorescent dots corresponding to the arteriolar emboli (Fig. 1C). A third embolus on the central retinal artery trunk, which had been overlooked on
Please cite this article in press as: Bacquet J-L, et al. Fundus autofluorescence in retinal artery occlusion: A more precise diagnosis. J Fr Ophtalmol (2017), http://dx.doi.org/10.1016/j.jfo.2017.03.010
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Figure 1. Case 1. A. Retinography of the left eye showing 2 arteriolar emboli along the inferotemporal arcade (arrowheads) and ischemic edema of the retina. B. Retinography 15 days after: barely visible embolus at the level of the trunk of the central retinal artery. C. Fundus autofluorescence: hypoautofluorescence of the ischemic zone and hyperautofluorescence of the retinal emboli. D. Fluorescein angiogram at the early phase: extensive non perfusion area.
the retinography (Fig. 1B), had appeared in the interval. This new embolic event led to reinforce the antiplatelet therapy. Fluorescein angiogram showed extensive area of non-perfusion (Fig. 1D), which was later treated by retinal panphotocoagulation.
cardiovascular work-up disclosed calcific aortic valve disease (Table 1). The pacemaker interrogation was positive for multiple atrial fibrillation episodes. Emboli could result either from aortic calcic emboli or from arrhythmia. Therefore, the cause of the retinal stroke could not be defined.
Case 2
Case 3
An 82-year-old woman was referred for a sudden loss of vision of the right eye. Her past history was positive for type 2 diabetes, hypertriglyceridemia and sinus node dysfunction treated with a pacemaker. She had a past history of bilateral macular degeneration. Fundus examination was blurry due to a dense cataract. However, It revealed macular exudates (Fig. 2A). There was no sign exudation on the macular OCT. Fundus autofluorescence showed a sharp hyperautofluorescence at the level of the superior hemitrunk of the central retinal artery (Fig. 2B). When examining carefully the retinography, this hyperautofluorescent zone matched with an arteriolar plaque (Fig. 2A, arrow), which was initially overlooked. Fluorescein angiogram revealed non-perfusion of the superotemporal retina, thus confirming the diagnosis of superior branch retinal artery occlusion. The
A 74-year-old pseudophakic man was referred for management of a central retinal artery occlusion of the right eye. The visual acuity was hand motion. He had a history of arterial hypertension, active tabagism (50 pack-years) and dyslipidemia. The fundus examination revealed a typical cherry-red spot within diffuse ischemic retinal edema, narrowed retinal arteries and a yellowish embolus at the level of the trunk of the retinal artery (Fig. 2C). Fundus autofluorescence showed macular hypoautofluorescence and revealed the embolus, which appeared as a sharp hyperautofluorescent spot (Fig. 2D). The cardiovascular work-up revealed a moderate right carotid stenosis (Table 1). The 24 h electrocardiogram and the echocardiogram were negative for cardiac cause of embolism. Brain MRI found a right thalamic infarction, however, neurologic examination was normal.
Please cite this article in press as: Bacquet J-L, et al. Fundus autofluorescence in retinal artery occlusion: A more precise diagnosis. J Fr Ophtalmol (2017), http://dx.doi.org/10.1016/j.jfo.2017.03.010
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J.-L. Bacquet et al. Table 1
Summary of clinical data, cardiovascular and neurologic workups.
Patient Age (years) Side of the Lens status retinal arterial occlusion
Cardiovascular Cardiovascular Neurologic risk factors workup workup
Presumed origin for the emboli
1
77
Left
Bilateral grade 2 corticonuclear cataract
Aortic and carotid atherosclerosis
2
82
Right
Bilateral grade 3 corticonuclear cataract
3
74
Right
Pseudophakic
Normal Severe right clinical carotid stenosis (ECST examination Brain CT 80%) Extensive angiography: aortic lacunar atheroscleinfarction of rotic plaques the right 24 h electrocaudate nucleus cardiogram: sinusal rhythm Echocardiogram: no intracardiac thrombus, normal ejection fraction Normal Treated hyper- Carotid clinical lipidemia plaques examination Hypertension without Normal brain Unbalanced stenosis type 2 Echocardiogram:CT severe calcific angiography diabetes (HbA1C: 7.9%) aortic valve stenosis Pacemaker interrogation: numerous atrial fibrillation episodes Right internal Normal Tobacco use clinical (50 PY) carotid Hyperlipidemia stenosis (ECST examination Brain MRI: left Hypertension 45%) Type 2 Extensive right thalamic infarction diabetes subclavian (HbA1C: 6%) plaques 24 h electrocardiogram: sinusal rhythm Echocardiogram: no intracardiac thrombus, normal ejection fraction Tobacco use (40 PY) Treated hyperlipidemia Hypertension
Not defined
Carotid atherosclerosis
PY: pack-year; ECST: European carotid surgery trial; CT: computed tomography; MRI: magnetic resonance imaging.
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Figure 2. A. Case 2. Retinography of the right eye. The fundus is blurred due to a dence corticonuclear cataract. An embolus is suspected at the level of the superior hemi-trunk of the central retinal artery (arrowhead). B. Case 2. Fundus autofluorescence: hyperautofluorescence of the embolus (arrowhead) and hypoautofluorescence of the ischemic macula. C. Case 3. Retinography of the right eye: typical cherry-red spot macula with visible embolus at the level of the trunk of the central retinal artery (arrowhead). D. Case 3. Fundus autofluorescence revealing the hyperautofluorescent embolus and the hypoautofluorescent ischemic retina.
Thus, this combined retinal and cerebral stroke was considered to be due to an atherosclerotic origin.
Discussion Funduscopic examination and retinography are not reliable to determine the nature of the emboli: both intra-observer and inter-observer agreement on the clinical qualitative assessment of retinal emboli is poor [6]. Moreover, fundus examination can be blurred by a dense cataract and altogether, retinal emboli are seen in less than half of the cases of retinal arterial occlusion [3]. Siddiqi et al. recently reported in a single clinical case that autofluorescence may highlight the retinal arterial emboli in RAO but did not discuss the underlying mechanism of autofluorescence of retinal emboli [8]. Moreover, autofluorescence shows hypofluorescence of the ischemic zones during the acute phase [9]. In the retina, the main fluorophore is lipofuscin, composed of lipid-containing residues of lysosomal digestion. Knowing that lipofuscin is found at high level in atherosclerotic plaques [10], it can be hypothesized that hyperautofluorescent emboli may originate from atherosclerotic plaques. However, Majstruk et al. recently
speculated that autofluorescence of retinal arterial plaques may be due to calcifications in the arterial wall [11]. In our series, 2 out of 3 patients with hyperautofluorescent emboli had evidence of an atherosclerotic origin of the vascular event. This case series confirms that fundus autofluorescence is a useful imaging technique for retinal artery occlusion and may help to detect arteriolar emboli. Although further studies, including patients with retinal emboli from various etiologies are warranted, fundus autofluorescence may help to define the nature of the retinal emboli, thus guiding the cardiovascular workup of this potentially lifethreatening disease.
Disclosure of interest The authors declare that they have no competing interest.
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Please cite this article in press as: Bacquet J-L, et al. Fundus autofluorescence in retinal artery occlusion: A more precise diagnosis. J Fr Ophtalmol (2017), http://dx.doi.org/10.1016/j.jfo.2017.03.010
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Please cite this article in press as: Bacquet J-L, et al. Fundus autofluorescence in retinal artery occlusion: A more precise diagnosis. J Fr Ophtalmol (2017), http://dx.doi.org/10.1016/j.jfo.2017.03.010