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Graefe's Archive for Clinical and Experimental Ophthalmology

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01-03-2020 | Macular Degeneration | Retinal Disorders

Linear and planar reflection artifacts on swept-source and spectral-domain optical coherence tomography due to hyperreflective crystalline deposits

Authors: Serena Fragiotta, Pedro Fernández-Avellaneda, Mark P. Breazzano, Lawrence A. Yannuzzi, Christine A. Curcio, K. Bailey Freund

Published in: Graefe's Archive for Clinical and Experimental Ophthalmology | Issue 3/2020

Abstract

Purpose

To describe novel spectral-domain (SD) and swept-source (SS) optical coherence tomography (OCT) linear and planar reflection artifacts produced by hyperreflective crystalline deposits (HCD).

Methods

Imaging from 10 eyes with HCD producing linear and planar artifacts on OCT was retrospectively analyzed. All eyes had SD-OCT (Spectralis HRA + OCT, Heidelberg Engineering, Germany) and SS-OCT angiography (PLEX Elite 9000, Carl Zeiss Meditec, Inc., Dublin, CA) acquired on the same day. The horizontal extent of planar artifacts and the corresponding HCD on B-scans was measured using a digital caliper. Artifact features from HCD in eyes with non-neovascular age-related macular degeneration (AMD) were analyzed and compared to those seen in two eyes with the “onion sign,” an OCT signature previously shown to represent cholesterol crystals (CC) in the sub-retinal pigment epithelium-basal laminar space of eyes with neovascular AMD. A third eye with the “onion sign” was imaged with dense B-scan (DB)-OCTA.

Results

Ten eyes of ten patients (77.4 ± 8.7 years) with HCD were analyzed. On SS-OCTA, HCD produced linear artifacts of high signal intensity passing through the HCD and spanning the entire scan depth. On SD-OCT, HCD produced planar artifacts located anterior to both the retina and a hyporeflective space representing normal vitreous signal. The horizontal extent of the artifact did not differ significantly from the corresponding HCD on OCT B-scans (P = 0.62). The OCT artifacts produced by the “onion sign” appeared similar to those of HCD. The additional eye with neovascular AMD imaged with DB-OCTA was characterized by a single, vertical, linear false-flow signal crossing retinal layers.

Conclusions

To the authors’ knowledge, this is the first description of SD- and SS-OCT/OCTA artifacts corresponding to both HCD and the “onion sign.” These artifacts are likely due to highly reflective CC previously shown on histology to correspond to both of these OCT signatures.

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Fragiotta S, Fernandez-Avellaneda P, Breazzano MP, Curcio CA, Leong BCS, Kato K, Yannuzzi LA, Freund KB (2019) The fate and prognostic implications of Hyperreflective crystalline deposits in Nonneovascular age-related macular degeneration. Invest Ophthalmol Vis Sci 60:3100–3109. https://doi.org/10.1167/iovs.19-26589 CrossRefPubMed

Christakopoulos C, Pryds A, Larsen M (2013) Subretinal lamellar bodies in polypoidal choroidal vasculopathy. Acta Ophthalmol 91:e248–e249. https://doi.org/10.1111/aos.12000 CrossRefPubMed

Nishimura S, Ehara S, Hasegawa T, Matsumoto K, Yoshikawa J, Shimada K (2017) Cholesterol crystal as a new feature of coronary vulnerable plaques: An optical coherence tomography study. J Cardiol 69:253–259. https://doi.org/10.1016/j.jjcc.2016.04.003 CrossRefPubMed

Margo CE, Pusateri TJ, Ulshafer RJ, Keller RK (1990) Lipid crystals in malignant melanoma of the choroid. Retina 10:68–71CrossRefPubMed

Ong SS, Cummings TJ, Vajzovic L, Mruthyunjaya P, Toth CA (2018) Comparison of optical coherence tomography with fundus photographs, fluorescein angiography, and histopathologic analysis in assessing coats disease. JAMA Ophthalmol. https://doi.org/10.1001/jamaophthalmol.2018.5654 CrossRefPubMed

Tsui I, Pineles SL (2018) What coats disease and age-related macular degeneration have in common. JAMA Ophthalmol. https://doi.org/10.1001/jamaophthalmol.2018.5645 CrossRefPubMed

Manschot WA, de Bruijn WC (1967) Coats's disease: definition and pathogenesis. Br J Ophthalmol 51:145–157CrossRefPubMedPubMedCentral

Pang CE, Messinger JD, Zanzottera EC, Freund KB, Curcio CA (2015) The onion sign in neovascular age-related macular degeneration represents cholesterol crystals. Ophthalmology 122:2316–2326. https://doi.org/10.1016/j.ophtha.2015.07.008 CrossRefPubMed

Li M, Dolz-Marco R, Messinger JD, Sloan KR, Ferrara D, Curcio CA, Freund KB (2019) Clinicopathologic correlation of aneurysmal type 1 neovascularization in age-related macular degeneration. Ophthalmol Retina 3:99–111. https://doi.org/10.1016/j.oret.2018.08.008 CrossRefPubMed

10.

Li M, Dolz-Marco R, Huisingh C, Messinger JD, Feist RM, Ferrara D, Freund KB, Curcio CA (2019) Clinicopathologic correlation of geographic atrophy secondary to age-related macular degeneration. Retina 39:802–816. https://doi.org/10.1097/IAE.0000000000002461 CrossRefPubMedPubMedCentral

11.

Wang RK, Jacques SL, Ma Z, Hurst S, Hanson SR, Gruber A (2007) Three dimensional optical angiography. Opt Express 15:4083–4097. https://doi.org/10.1364/oe.15.004083 CrossRefPubMed

12.

An L, Wang RK (2008) In vivo volumetric imaging of vascular perfusion within human retina and choroids with optical micro-angiography. Opt Express 16:11438–11452. https://doi.org/10.1364/oe.16.011438 CrossRefPubMed

13.

de Carlo TE, Bonini Filho MA, Chin AT, Adhi M, Ferrara D, Baumal CR, Witkin AJ, Reichel E, Duker JS, Waheed NK (2015) Spectral-domain optical coherence tomography angiography of choroidal neovascularization. Ophthalmology 122:1228–1238. https://doi.org/10.1016/j.ophtha.2015.01.029 CrossRefPubMed

14.

Ghasemi Falavarjani K, Al-Sheikh M, Akil H, Sadda SR (2017) Image artefacts in swept-source optical coherence tomography angiography. Br J Ophthalmol 101:564–568. https://doi.org/10.1136/bjophthalmol-2016-309104 CrossRefPubMed

15.

Enders C, Lang GE, Dreyhaupt J, Loidl M, Lang GK, Werner JU (2019) Quantity and quality of image artifacts in optical coherence tomography angiography. PLoS One 14:e0210505. https://doi.org/10.1371/journal.pone.0210505 CrossRefPubMedPubMedCentral

16.

Wu CT, Tsai MT, Lee CK (2014) Two-level optical coherence tomography scheme for suppressing spectral saturation artifacts. Sensors (Basel) 14:13548–13555. https://doi.org/10.3390/s140813548 CrossRef

17.

Zheng K, Liu B, Huang C, Brezinski ME (2008) Experimental confirmation of potential swept source optical coherence tomography performance limitations. Appl Opt 47:6151–6158CrossRefPubMedPubMedCentral

18.

Cover KL, Slasky BS, Skolnick ML (1985) Sonography of cholesterol in the biliary system. J Ultrasound Med 4:647–653CrossRefPubMed

19.

Ozan E, Atac GK (2001) Gundogdu S (2016) twinkling artifact on color Doppler ultrasound: an advantage or a pitfall? J Med Ultrason 43:361–371. https://doi.org/10.1007/s10396-016-0715-z CrossRef

20.

Tchelepi H, Ralls PW (2009) Color comet-tail artifact: clinical applications. AJR Am J Roentgenol 192:11–18. https://doi.org/10.2214/AJR.07.3893 CrossRefPubMed

21.

Rahmouni A, Bargoin R, Herment A, Bargoin N, Vasile N (1996) Color Doppler twinkling artifact in hyperechoic regions. Radiology 199:269–271. https://doi.org/10.1148/radiology.199.1.8633158 CrossRefPubMed

22.

Kamaya A, Tuthill T, Rubin JM (2003) Twinkling artifact on color Doppler sonography: dependence on machine parameters and underlying cause. AJR Am J Roentgenol 180:215–222. https://doi.org/10.2214/ajr.180.1.1800215 CrossRefPubMed

23.

Querques G, Georges A, Ben Moussa N, Sterkers M, Souied EH (2014) Appearance of regressing drusen on optical coherence tomography in age-related macular degeneration. Ophthalmology 121:173–179. https://doi.org/10.1016/j.ophtha.2013.06.024 CrossRefPubMed

24.

Tan ACS, Pilgrim MG, Fearn S, Bertazzo S, Tsolaki E, Morrell AP, Li M, Messinger JD, Dolz-Marco R, Lei J, Nittala MG, Sadda SR, Lengyel I, Freund KB, Curcio CA (2018) Calcified nodules in retinal drusen are associated with disease progression in age-related macular degeneration. Sci Transl Med:10. https://doi.org/10.1126/scitranslmed.aat4544 CrossRefPubMed

25.

Suzuki M, Curcio CA, Mullins RF, Spaide RF (2015) Refractile drusen: clinical imaging and candidate histology. Retina 35:859–865. https://doi.org/10.1097/IAE.0000000000000503 CrossRefPubMed

26.

Cukras C, Agron E, Klein ML, Ferris FL 3rd, Chew EY, Gensler G, Wong WT, Age-Related Eye Disease Study Research G (2010) Natural history of drusenoid pigment epithelial detachment in age-related macular degeneration: age-related eye disease study report no. 28. Ophthalmology 117:489–499. https://doi.org/10.1016/j.ophtha.2009.12.002 CrossRefPubMed

27.

Hassenstein A, Meyer CH (2009) Clinical use and research applications of Heidelberg retinal angiography and spectral-domain optical coherence tomography - a review. Clin Exp Ophthalmol 37:130–143. https://doi.org/10.1111/j.1442-9071.2009.02017.x CrossRefPubMed

28.

Freund KB, Gattoussi S, Leong BCS (2018) Dense B-scan optical coherence tomography angiography. Am J Ophthalmol 190:78–88. https://doi.org/10.1016/j.ajo.2018.03.029 CrossRefPubMed

29.

Green WR, Key SN 3rd (1977) Senile macular degeneration: a histopathologic study. Trans Am Ophthalmol Soc 75:180–254PubMedPubMedCentral

30.

Fleckenstein M, Charbel Issa P, Helb HM, Schmitz-Valckenberg S, Finger RP, Scholl HP, Loeffler KU, Holz FG (2008) High-resolution spectral domain-OCT imaging in geographic atrophy associated with age-related macular degeneration. Invest Ophthalmol Vis Sci 49:4137–4144. https://doi.org/10.1167/iovs.08-1967 CrossRefPubMed

31.

Moussa K, Lee JY, Stinnett SS, Jaffe GJ (2013) Spectral domain optical coherence tomography-determined morphologic predictors of age-related macular degeneration-associated geographic atrophy progression. Retina 33:1590–1599. https://doi.org/10.1097/IAE.0b013e31828d6052 CrossRefPubMed

32.

Curcio CA, Millican CL, Bailey T, Kruth HS (2001) Accumulation of cholesterol with age in human Bruch's membrane. Invest Ophthalmol Vis Sci 42:265–274PubMed

33.

Malek G, Li CM, Guidry C, Medeiros NE, Curcio CA (2003) Apolipoprotein B in cholesterol-containing drusen and basal deposits of human eyes with age-related maculopathy. Am J Pathol 162:413–425. https://doi.org/10.1016/S0002-9440(10)63836-9 CrossRefPubMedPubMedCentral

34.

Sarks JP, Sarks SH, Killingsworth MC (1988) Evolution of geographic atrophy of the retinal pigment epithelium. Eye (Lond) 2(Pt 5):552–577. https://doi.org/10.1038/eye.1988.106 CrossRef

35.

Sarks JP, Sarks SH, Killingsworth MC (1994) Evolution of soft drusen in age-related macular degeneration. Eye (Lond) 8(Pt 3):269–283. https://doi.org/10.1038/eye.1994.57 CrossRef

36.

Curcio CA, Johnson M, Huang JD, Rudolf M (2009) Aging, age-related macular degeneration, and the response-to-retention of apolipoprotein B-containing lipoproteins. Prog Retin Eye Res 28:393–422. https://doi.org/10.1016/j.preteyeres.2009.08.001 CrossRefPubMedPubMedCentral

37.

Curcio CA (2018) Soft drusen in age-related macular degeneration: biology and targeting via the oil spill strategies. Invest Ophthalmol Vis Sci 59:AMD160–AMD181. https://doi.org/10.1167/iovs.18-24882 CrossRefPubMedPubMedCentral

38.

Phelps P, Steele AD, McCarty DJ Jr (1968) Compensated polarized light microscopy. Identification of crystals in synovial fluids from gout and pseudogout. JAMA 203:508–512CrossRefPubMed

39.

Weller RO, Rodger FC (1980) Crystalline stromal dystrophy: histochemistry and ultrastructure of the cornea. Br J Ophthalmol 64:46–52CrossRefPubMedPubMedCentral

40.

Glancy JJ, Goddard J, Pearson DE (1980) In vitro demonstration of cholesterol crystals' high echogenicity relative to protein particles. J Clin Ultrasound 8:27–29CrossRefPubMed

41.

Manjunath V, Taha M, Fujimoto JG, Duker JS (2010) Choroidal thickness in normal eyes measured using cirrus HD optical coherence tomography. Am J Ophthalmol 150(325–329):e321. https://doi.org/10.1016/j.ajo.2010.04.018 CrossRef

42.

Suhalim JL, Chung CY, Lilledahl MB, Lim RS, Levi M, Tromberg BJ, Potma EO (2012) Characterization of cholesterol crystals in atherosclerotic plaques using stimulated Raman scattering and second-harmonic generation microscopy. Biophys J 102:1988–1995. https://doi.org/10.1016/j.bpj.2012.03.016 CrossRefPubMedPubMedCentral

43.

Potsaid B, Baumann B, Huang D, Barry S, Cable AE, Schuman JS, Duker JS, Fujimoto JG (2010) Ultrahigh speed 1050nm swept source/Fourier domain OCT retinal and anterior segment imaging at 100,000 to 400,000 axial scans per second. Opt Express 18:20029–20048. https://doi.org/10.1364/OE.18.020029 CrossRefPubMed

44.

Pichi F, Massaro D, Serafino M, Carrai P, Giuliari GP, Shields CL, Veronese C, Ciardella AP, Nucci P (2016) RETINAL ASTROCYTIC HAMARTOMA: optical coherence tomography classification and correlation with tuberous sclerosis complex. Retina 36:1199–1208. https://doi.org/10.1097/IAE.0000000000000829 CrossRefPubMed

45.

Sato T, Mrejen S, Spaide RF (2013) Multimodal imaging of optic disc drusen. Am J Ophthalmol 156(275–282):e271. https://doi.org/10.1016/j.ajo.2013.03.039 CrossRef

46.

Shields CL, Benevides R, Materin MA, Shields JA (2006) Optical coherence tomography of retinal astrocytic hamartoma in 15 cases. Ophthalmology 113:1553–1557. https://doi.org/10.1016/j.ophtha.2006.03.032 CrossRefPubMed

47.

Shields CL, Say EAT, Fuller T, Arora S, Samara WA, Shields JA (2016) Retinal Astrocytic Hamartoma arises in nerve Fiber layer and shows "moth-eaten" optically empty spaces on optical coherence tomography. Ophthalmology 123:1809–1816. https://doi.org/10.1016/j.ophtha.2016.04.011 CrossRefPubMed

48.

Freton A, Finger PT (2012) Spectral domain-optical coherence tomography analysis of choroidal osteoma. Br J Ophthalmol 96:224–228. https://doi.org/10.1136/bjo.2011.202408 CrossRefPubMed

49.

Pellegrini M, Invernizzi A, Giani A, Staurenghi G (2014) Enhanced depth imaging optical coherence tomography features of choroidal osteoma. Retina 34:958–963. https://doi.org/10.1097/IAE.0000000000000017 CrossRefPubMed

50.

Kataoka Y, Puri R, Hammadah M, Duggal B, Uno K, Kapadia SR, Tuzcu EM, Nissen SE, Nicholls SJ (2015) Cholesterol crystals associate with coronary plaque vulnerability in vivo. J Am Coll Cardiol 65:630–632. https://doi.org/10.1016/j.jacc.2014.11.039 CrossRefPubMed

51.

Abela GS, Aziz K (2006) Cholesterol crystals rupture biological membranes and human plaques during acute cardiovascular events--a novel insight into plaque rupture by scanning electron microscopy. Scanning 28:1–10CrossRefPubMed

52.

Tan ACS, Astroz P, Dansingani KK, Slakter JS, Yannuzzi LA, Curcio CA, Freund KB (2017) The evolution of the plateau, an optical coherence tomography signature seen in geographic atrophy. Invest Ophthalmol Vis Sci 58:2349–2358. https://doi.org/10.1167/iovs.16-21237 CrossRefPubMedPubMedCentral

Title: Linear and planar reflection artifacts on swept-source and spectral-domain optical coherence tomography due to hyperreflective crystalline deposits
Authors: Serena Fragiotta
Pedro Fernández-Avellaneda
Mark P. Breazzano
Lawrence A. Yannuzzi
Christine A. Curcio
K. Bailey Freund
Publication date: 01-03-2020
Publisher: Springer Berlin Heidelberg
Keyword: Macular Degeneration
Published in: Graefe's Archive for Clinical and Experimental Ophthalmology / Issue 3/2020
Print ISSN: 0721-832X
Electronic ISSN: 1435-702X
DOI: https://doi.org/10.1007/s00417-019-04565-y

At a glance: The STEP trials

Springer Medicine

Linear and planar reflection artifacts on swept-source and spectral-domain optical coherence tomography due to hyperreflective crystalline deposits

Abstract

Purpose

Methods

Results

Conclusions

At a glance: The STEP trials

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

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