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Published in: Graefe's Archive for Clinical and Experimental Ophthalmology 4/2017

01-04-2017 | Retinal Disorders

Deep and superficial OCT angiography changes after macular peeling: idiopathic vs diabetic epiretinal membranes

Authors: Mario R. Romano, Gilda Cennamo, Stefano Schiemer, Claudia Rossi, Federica Sparnelli, Giovanni Cennamo

Published in: Graefe's Archive for Clinical and Experimental Ophthalmology | Issue 4/2017

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Abstract

Background

To assess changes in deep and superficial perifoveal capillary plexus after macular peeling in idiopathic and diabetic epiretinal membrane (iERM and dERM, respectively).

Methods

Cross-sectional comparative study. We included 40 eyes from 40 patients affected by iERM (20 eyes) and dERM (20 eyes), as well as 34 eyes from 17 healthy, age-matched patients. Patients received a complete ophthalmic evaluation including axial and en-face scanning spectral-domain analysis, optical coherence tomography angiography, and microperimetry. Split-spectrum amplitude-decorrelation angiography images were obtained to quantify the deep and superficial layers of perifoveal capillary-free zone (CFZ). The main outcome measures were: (i) differences at baseline between deep and superficial CFZ in iERM and dERM vs control, and (ii) changes in deep and superficial CFZ plexus after surgery in iERM vs dERM.

Results

The deep CFZ only significantly increased in dERM at the end of the follow-up period (6 months). No statistically significant differences were found between preoperative and postoperative superficial vascular plexus in iERM or dERM. At the end of the follow-up, statistically significant differences between preoperative and postoperative ganglion cell complex (GCC) average were found only in the iERM group. Best-corrected visual acuity significantly improved after surgery both in the iERM (P = 0.0053) and dERM (P < 0.0001) groups. After 6 months, macular sensitivity increased in the iERM group, but there was no statistically significant change in the dERM group.

Conclusions

In dERM, the deep CFZ significantly increases after ILM peeling, whereas postoperative angiography changes were not significant in iERM. This could be because the impaired diabetic perifoveal capillary plexus are more sensitive to the iatrogenic damage to Müller cells, induced by peeling.
Literature
1.
go back to reference Gupta P, Yee KM, Garcia P et al (2011) Vitreoschisis in macular diseases. Br J Ophthalmol 95:376–380CrossRefPubMed Gupta P, Yee KM, Garcia P et al (2011) Vitreoschisis in macular diseases. Br J Ophthalmol 95:376–380CrossRefPubMed
2.
go back to reference Bu SC, Kuijer R, Li XR, Hooymans JM, Los LI (2014) Idiopathic epiretinal membrane. Retina 34:2317–2335CrossRefPubMed Bu SC, Kuijer R, Li XR, Hooymans JM, Los LI (2014) Idiopathic epiretinal membrane. Retina 34:2317–2335CrossRefPubMed
3.
go back to reference Kritzenberger M, Junglas B, Framme C et al (2011) Different collagen types define two types of idiopathic epiretinal membranes. Histopathology 58:953–965CrossRefPubMed Kritzenberger M, Junglas B, Framme C et al (2011) Different collagen types define two types of idiopathic epiretinal membranes. Histopathology 58:953–965CrossRefPubMed
4.
go back to reference Bringmann A, Wiedemann P (2009) Involvement of Müller glial cells in epiretinal membrane formation. Graefes Arch Clin Exp Ophthalmol 247:865–883CrossRefPubMed Bringmann A, Wiedemann P (2009) Involvement of Müller glial cells in epiretinal membrane formation. Graefes Arch Clin Exp Ophthalmol 247:865–883CrossRefPubMed
5.
go back to reference Smiddy WE, Maguire AM, Green WR et al (1989) Idiopathic epiretinal membranes. Ultrastructural characteristics and clinicopathologic correlation. Ophthalmology 96:811–820, discussion 821CrossRefPubMed Smiddy WE, Maguire AM, Green WR et al (1989) Idiopathic epiretinal membranes. Ultrastructural characteristics and clinicopathologic correlation. Ophthalmology 96:811–820, discussion 821CrossRefPubMed
6.
go back to reference Zhao F, Gandorfer A, Haritoglou C et al (2013) Epiretinal cell proliferation in macular pucker and vitreomacular traction syndrome: analysis of flat-mounted internal limiting membrane specimens. Retina 33:77–88CrossRefPubMed Zhao F, Gandorfer A, Haritoglou C et al (2013) Epiretinal cell proliferation in macular pucker and vitreomacular traction syndrome: analysis of flat-mounted internal limiting membrane specimens. Retina 33:77–88CrossRefPubMed
7.
go back to reference Steel DH, Lotery AJ (2013) Idiopathic vitreomacular traction and macular hole: a comprehensive review of pathophysiology, diagnosis, and treatment. Eye 27 Suppl 1:S1–S21CrossRefPubMed Steel DH, Lotery AJ (2013) Idiopathic vitreomacular traction and macular hole: a comprehensive review of pathophysiology, diagnosis, and treatment. Eye 27 Suppl 1:S1–S21CrossRefPubMed
8.
go back to reference Snead DR, James S, Snead MP (2008) Pathological changes in the vitreoretinal junction 1: epiretinal membrane formation. Eye 22:1310–1317CrossRefPubMed Snead DR, James S, Snead MP (2008) Pathological changes in the vitreoretinal junction 1: epiretinal membrane formation. Eye 22:1310–1317CrossRefPubMed
9.
go back to reference Kampik A (2012) Pathology of epiretinal membrane, idiopathic macular hole, and vitreomacular traction syndrome. Retina 32 Suppl 2:S194–S198, discussion S198–199CrossRefPubMed Kampik A (2012) Pathology of epiretinal membrane, idiopathic macular hole, and vitreomacular traction syndrome. Retina 32 Suppl 2:S194–S198, discussion S198–199CrossRefPubMed
10.
go back to reference Junemann AG, Rejdak R, Huchzermeyer C et al (2015) Elevated vitreous body glial fibrillary acidic protein in retinal diseases. Graefes Arch Clin Exp Ophthalmol 253:2181–2186CrossRefPubMedPubMedCentral Junemann AG, Rejdak R, Huchzermeyer C et al (2015) Elevated vitreous body glial fibrillary acidic protein in retinal diseases. Graefes Arch Clin Exp Ophthalmol 253:2181–2186CrossRefPubMedPubMedCentral
11.
go back to reference Ripandelli G, Scarinci F, Piaggi P et al (2015) Macular pucker: to peel or not to peel the internal limiting membrane? A microperimetric response. Retina 35:498–507CrossRefPubMed Ripandelli G, Scarinci F, Piaggi P et al (2015) Macular pucker: to peel or not to peel the internal limiting membrane? A microperimetric response. Retina 35:498–507CrossRefPubMed
12.
go back to reference Spaide RF, Klancnik JM Jr, Cooney MJ (2015) Retinal vascular layers imaged by fluorescein angiography and optical coherence tomography angiography. JAMA Ophthalmol 133:45–50CrossRefPubMed Spaide RF, Klancnik JM Jr, Cooney MJ (2015) Retinal vascular layers imaged by fluorescein angiography and optical coherence tomography angiography. JAMA Ophthalmol 133:45–50CrossRefPubMed
13.
go back to reference Di G, Weihong Y, Xiao Z et al (2015) A morphological study of the foveal avascular zone in patients with diabetes mellitus using optical coherence tomography angiography. Graefes Arch Clin Exp Ophthalmol 254(5):873–879CrossRefPubMed Di G, Weihong Y, Xiao Z et al (2015) A morphological study of the foveal avascular zone in patients with diabetes mellitus using optical coherence tomography angiography. Graefes Arch Clin Exp Ophthalmol 254(5):873–879CrossRefPubMed
14.
go back to reference Ishibazawa A, Nagaoka T, Takahashi A et al (2015) Optical coherence tomography angiography in diabetic retinopathy: a prospective pilot study. Am J Ophthalmol 160:c–44.e31 Ishibazawa A, Nagaoka T, Takahashi A et al (2015) Optical coherence tomography angiography in diabetic retinopathy: a prospective pilot study. Am J Ophthalmol 160:c–44.e31
15.
go back to reference Crossland MD, Dunbar HM, Rubin GS (2009) Fixation stability measurement using the MP1 microperimeter. Retina 29:651–656CrossRefPubMed Crossland MD, Dunbar HM, Rubin GS (2009) Fixation stability measurement using the MP1 microperimeter. Retina 29:651–656CrossRefPubMed
16.
go back to reference Fujii GY, De Juan E Jr, Sunness J, Humayun MS, Pieramici DJ, Chang TS (2002) Patient selection for macular translocation surgery using the scanning laser ophthalmoscope. Ophthalmology 109:1737–1744CrossRefPubMed Fujii GY, De Juan E Jr, Sunness J, Humayun MS, Pieramici DJ, Chang TS (2002) Patient selection for macular translocation surgery using the scanning laser ophthalmoscope. Ophthalmology 109:1737–1744CrossRefPubMed
17.
go back to reference Midena E, Radin PP, Pilotto E, Ghirlando A, Convento E, Varano M (2004) Fixation pattern and macular sensitivity in eyes with subfoveal choroidal neovascularization secondary to age-related macular degeneration. A microperimetry study. Semin Ophthalmol 19:55–61CrossRefPubMed Midena E, Radin PP, Pilotto E, Ghirlando A, Convento E, Varano M (2004) Fixation pattern and macular sensitivity in eyes with subfoveal choroidal neovascularization secondary to age-related macular degeneration. A microperimetry study. Semin Ophthalmol 19:55–61CrossRefPubMed
18.
go back to reference Scarinci F, Jampol LM, Linsenmeier RA, Fawzi AA (2015) Association of diabetic macular nonperfusion with outer retinal disruption on optical coherence tomography. JAMA Ophthalmol 133:1036–1044CrossRefPubMedPubMedCentral Scarinci F, Jampol LM, Linsenmeier RA, Fawzi AA (2015) Association of diabetic macular nonperfusion with outer retinal disruption on optical coherence tomography. JAMA Ophthalmol 133:1036–1044CrossRefPubMedPubMedCentral
19.
go back to reference Kenawy N, Wong D, Stappler T et al (2010) Does the presence of an epiretinal membrane alter the cleavage plane during internal limiting membrane peeling? Ophthalmology 117:320–323.e1CrossRefPubMed Kenawy N, Wong D, Stappler T et al (2010) Does the presence of an epiretinal membrane alter the cleavage plane during internal limiting membrane peeling? Ophthalmology 117:320–323.e1CrossRefPubMed
20.
go back to reference Romano MR, Vallejo-Garcia JL, Camesasca FI, Vinciguerra P, Costagliola C (2012) Vitreo-papillary adhesion as a prognostic factor in pseudo- and lamellar macular holes. Eye 26:810–815CrossRefPubMedPubMedCentral Romano MR, Vallejo-Garcia JL, Camesasca FI, Vinciguerra P, Costagliola C (2012) Vitreo-papillary adhesion as a prognostic factor in pseudo- and lamellar macular holes. Eye 26:810–815CrossRefPubMedPubMedCentral
21.
go back to reference Arend O, Wolf S, Jung F et al (1991) Retinal microcirculation in patients with diabetes mellitus: dynamic and morphological analysis of perifoveal capillary network. Br J Ophthalmol 75:514–518CrossRefPubMedPubMedCentral Arend O, Wolf S, Jung F et al (1991) Retinal microcirculation in patients with diabetes mellitus: dynamic and morphological analysis of perifoveal capillary network. Br J Ophthalmol 75:514–518CrossRefPubMedPubMedCentral
22.
go back to reference Sander B, Larsen M, Engler C, Lund-Andersen H, Parving HH (1994) Early changes in diabetic retinopathy: capillary loss and blood–retina barrier permeability in relation to metabolic control. Acta Ophthalmol 72:553–559CrossRef Sander B, Larsen M, Engler C, Lund-Andersen H, Parving HH (1994) Early changes in diabetic retinopathy: capillary loss and blood–retina barrier permeability in relation to metabolic control. Acta Ophthalmol 72:553–559CrossRef
23.
go back to reference Pierro L, Iuliano L, Gagliardi M, Codenotti M, Ambrosi A, Bandello F (2015) Role of ganglion cell complex in visual recovery following surgical internal limiting membrane peeling. Graefes Arch Clin Exp Ophthalmol 253:37–45CrossRefPubMed Pierro L, Iuliano L, Gagliardi M, Codenotti M, Ambrosi A, Bandello F (2015) Role of ganglion cell complex in visual recovery following surgical internal limiting membrane peeling. Graefes Arch Clin Exp Ophthalmol 253:37–45CrossRefPubMed
24.
go back to reference Barber AJ (2003) A new view of diabetic retinopathy: a neurodegenerative disease of the eye. Prog Neuropsychopharmacol Biol Psychiatry 27:283–290CrossRefPubMed Barber AJ (2003) A new view of diabetic retinopathy: a neurodegenerative disease of the eye. Prog Neuropsychopharmacol Biol Psychiatry 27:283–290CrossRefPubMed
25.
go back to reference Lieth E, Gardner TW, Barber AJ, Antonetti DA (2000) Penn State retina research G. Retinal neurodegeneration: early pathology in diabetes. Clin Experiment Ophthalmol 28:3–8CrossRefPubMed Lieth E, Gardner TW, Barber AJ, Antonetti DA (2000) Penn State retina research G. Retinal neurodegeneration: early pathology in diabetes. Clin Experiment Ophthalmol 28:3–8CrossRefPubMed
26.
go back to reference Gella L, Raman R, Kulothungan V, Saumya Pal S, Ganesan S, Sharma T (2015) Retinal sensitivity in subjects with type 2 diabetes mellitus: Sankara Nethralaya Diabetic Retinopathy Epidemiology and Molecular Genetics Study (SN-DREAMS II, Report No. 4). Br J Ophthalmol. doi:10.1136/bjophthalmol-2015-307064 PubMed Gella L, Raman R, Kulothungan V, Saumya Pal S, Ganesan S, Sharma T (2015) Retinal sensitivity in subjects with type 2 diabetes mellitus: Sankara Nethralaya Diabetic Retinopathy Epidemiology and Molecular Genetics Study (SN-DREAMS II, Report No. 4). Br J Ophthalmol. doi:10.​1136/​bjophthalmol-2015-307064 PubMed
27.
go back to reference Verma A, Rani PK, Raman R et al (2009) Is neuronal dysfunction an early sign of diabetic retinopathy? Microperimetry and spectral domain optical coherence tomography (SD-OCT) study in individuals with diabetes, but no diabetic retinopathy. Eye 23:1824–1830CrossRefPubMed Verma A, Rani PK, Raman R et al (2009) Is neuronal dysfunction an early sign of diabetic retinopathy? Microperimetry and spectral domain optical coherence tomography (SD-OCT) study in individuals with diabetes, but no diabetic retinopathy. Eye 23:1824–1830CrossRefPubMed
28.
go back to reference Verma A, Raman R, Vaitheeswaran K et al (2012) Does neuronal damage precede vascular damage in subjects with type 2 diabetes mellitus and having no clinical diabetic retinopathy? Ophthalmic Res 47:202–207CrossRefPubMed Verma A, Raman R, Vaitheeswaran K et al (2012) Does neuronal damage precede vascular damage in subjects with type 2 diabetes mellitus and having no clinical diabetic retinopathy? Ophthalmic Res 47:202–207CrossRefPubMed
29.
go back to reference Lee JW, Kim IT (2010) Outcomes of idiopathic macular epiretinal membrane removal with and without internal limiting membrane peeling: a comparative study. Jpn J Ophthalmol 54:129–134CrossRefPubMed Lee JW, Kim IT (2010) Outcomes of idiopathic macular epiretinal membrane removal with and without internal limiting membrane peeling: a comparative study. Jpn J Ophthalmol 54:129–134CrossRefPubMed
30.
go back to reference Tadayoni R, Paques M, Massin P et al (2001) Dissociated optic nerve fiber layer appearance of the fundus after idiopathic epiretinal membrane removal. Ophthalmology 108:2279–2283CrossRefPubMed Tadayoni R, Paques M, Massin P et al (2001) Dissociated optic nerve fiber layer appearance of the fundus after idiopathic epiretinal membrane removal. Ophthalmology 108:2279–2283CrossRefPubMed
31.
go back to reference Ito Y, Terasaki H, Takahashi A et al (2005) Dissociated optic nerve fiber layer appearance after internal limiting membrane peeling for idiopathic macular holes. Ophthalmology 112:1415–1420CrossRefPubMed Ito Y, Terasaki H, Takahashi A et al (2005) Dissociated optic nerve fiber layer appearance after internal limiting membrane peeling for idiopathic macular holes. Ophthalmology 112:1415–1420CrossRefPubMed
32.
go back to reference Lazzeri S, Piaggi P, Parravano M et al (2013) Analysis of functional dissociations between best corrected visual acuity and microperimetric parameters in neovascular age-related macular degeneration patients underwent to three monthly ranibizumab injections. Clin Experiment Ophthalmol 4:4 Lazzeri S, Piaggi P, Parravano M et al (2013) Analysis of functional dissociations between best corrected visual acuity and microperimetric parameters in neovascular age-related macular degeneration patients underwent to three monthly ranibizumab injections. Clin Experiment Ophthalmol 4:4
33.
go back to reference Shahlaee A, Pefkianaki M, Hsu J, Ho AC (2016) Measurement of foveal avascular zone dimensions and its reliability in healthy eyes using optical coherence tomography angiography. Am J Ophthalmol 161:50.e1–55.e1CrossRef Shahlaee A, Pefkianaki M, Hsu J, Ho AC (2016) Measurement of foveal avascular zone dimensions and its reliability in healthy eyes using optical coherence tomography angiography. Am J Ophthalmol 161:50.e1–55.e1CrossRef
34.
go back to reference Carpineto P, Mastropasqua R, Marchini G, Toto L, Di Nicola M, Di Antonio L (2015) Reproducibility and repeatability of foveal avascular zone measurements in healthy subjects by optical coherence tomography angiography. Br J Ophthalmol 100:671–676CrossRefPubMed Carpineto P, Mastropasqua R, Marchini G, Toto L, Di Nicola M, Di Antonio L (2015) Reproducibility and repeatability of foveal avascular zone measurements in healthy subjects by optical coherence tomography angiography. Br J Ophthalmol 100:671–676CrossRefPubMed
Metadata
Title
Deep and superficial OCT angiography changes after macular peeling: idiopathic vs diabetic epiretinal membranes
Authors
Mario R. Romano
Gilda Cennamo
Stefano Schiemer
Claudia Rossi
Federica Sparnelli
Giovanni Cennamo
Publication date
01-04-2017
Publisher
Springer Berlin Heidelberg
Published in
Graefe's Archive for Clinical and Experimental Ophthalmology / Issue 4/2017
Print ISSN: 0721-832X
Electronic ISSN: 1435-702X
DOI
https://doi.org/10.1007/s00417-016-3534-4

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