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Published in: Japanese Journal of Ophthalmology 3/2020

01-05-2020 | Angiography | Clinical Investigation

Foveal avascular zone area analysis in juvenile-onset type 1 diabetes using optical coherence tomography angiography

Authors: Hajime Onoe, Yorihisa Kitagawa, Hiroyuki Shimada, Ari Shinojima, Masako Aoki, Tatsuhiko Urakami

Published in: Japanese Journal of Ophthalmology | Issue 3/2020

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Abstract

Purpose

Optical coherence tomography angiography (OCTA) was performed on patients with juvenile-onset type 1 diabetes (T1DM) but with no diabetic retinopathy to measure the foveal avascular zone (FAZ) area.

Study Design

Retrospective single-facility study

Methods

Twenty-nine patients (58 eyes) with juvenile-onset T1DM were studied. Images (3 mm x 3 mm cube centered on the fovea) were acquired using an OCTA device. Age at examination was 16.1 ± 8.7 years; onset age was 6.4 ± 3.5 years; duration of diabetes was 9.7 ± 8.3 years. Twenty-four age-matched healthy individuals were studied as controls.

Results

FAZ area was significantly larger in T1DM patients than in controls (0.29 ± 0.09 vs. 0.25 ± 0.08 mm2, P = 0.0234). Parafoveal vessel density was not significantly different between patients and controls (50.43 ± 4.24 vs. 50.07 ± 4.64, P = 0.8842). By generalized linear model analysis, annual HbA1c (P = 0.0190), number of serious hypoglycemic attacks (P = 0.0210), and onset age (P = 0.0447) were identified as variables significantly associated with FAZ area. Age, gender, duration of disease, total cholesterol, high or low-density lipoprotein, triglycerides, and body mass index were not significantly associated with FAZ area.

Conclusion

Patients with juvenile-onset T1DM and no diabetic retinopathy had increased FAZ, but no significant difference in parafoveal vessel density compared to healthy controls. Larger FAZ area was associated with higher annual HbA1c, more episodes of severe hypoglycemic attacks, and older onset age.
Literature
1.
go back to reference Lestradet H, Papoz L, Hellouin de Menibus C, Levavasseur F, Besse J, Billaud L, et al. Long-term study of mortality and vascular complications in juvenile-onset (type 1) diabetes. Diabetes. 1981;30:175–9.CrossRef Lestradet H, Papoz L, Hellouin de Menibus C, Levavasseur F, Besse J, Billaud L, et al. Long-term study of mortality and vascular complications in juvenile-onset (type 1) diabetes. Diabetes. 1981;30:175–9.CrossRef
2.
go back to reference Kang EY, Lo FS, Wang JP, Yeh LK, Wu AL, Tseng YJ, Chang Gung Juvenile Diabetes Eye Study Group, et al. Nomogram for prediction of non-proliferative diabetic retinopathy in juvenile-onset type 1 diabetes: a cohort study in an Asian population. Sci Rep. 2018;8:12164.CrossRef Kang EY, Lo FS, Wang JP, Yeh LK, Wu AL, Tseng YJ, Chang Gung Juvenile Diabetes Eye Study Group, et al. Nomogram for prediction of non-proliferative diabetic retinopathy in juvenile-onset type 1 diabetes: a cohort study in an Asian population. Sci Rep. 2018;8:12164.CrossRef
3.
go back to reference Wang NK, Lai CC, Wang JP, Wu WC, Liu L, Yeh LK, et al. Risk factors associated with the development of retinopathy 10 yr after the diagnosis of juvenile-onset type 1 diabetes in Taiwan: a cohort study from the CGJDES. Pediatr Diabetes. 2016;17:407–16.CrossRef Wang NK, Lai CC, Wang JP, Wu WC, Liu L, Yeh LK, et al. Risk factors associated with the development of retinopathy 10 yr after the diagnosis of juvenile-onset type 1 diabetes in Taiwan: a cohort study from the CGJDES. Pediatr Diabetes. 2016;17:407–16.CrossRef
4.
go back to reference Skrivarhaug T, Fosmark DS, Stene LC, Bangstad HJ, Sandvik L, Hanssen KF, et al. Low cumulative incidence of proliferative retinopathy in childhood-onset type 1 diabetes: a 24-year follow-up study. Diabetologia. 2006;49:2281–90.CrossRef Skrivarhaug T, Fosmark DS, Stene LC, Bangstad HJ, Sandvik L, Hanssen KF, et al. Low cumulative incidence of proliferative retinopathy in childhood-onset type 1 diabetes: a 24-year follow-up study. Diabetologia. 2006;49:2281–90.CrossRef
5.
go back to reference Donaghue KC, Marcovecchio ML, Wadwa RP, Chew EY, Wong TY, Calliari LE, et al. ISPAD Clinical Practice Consensus Guidelines 2018: Microvascular and macrovascular complications in children and adolescents. Pediatr Diabetes. 2018;27:262–74.CrossRef Donaghue KC, Marcovecchio ML, Wadwa RP, Chew EY, Wong TY, Calliari LE, et al. ISPAD Clinical Practice Consensus Guidelines 2018: Microvascular and macrovascular complications in children and adolescents. Pediatr Diabetes. 2018;27:262–74.CrossRef
6.
go back to reference Al-Sheikh M, Akil H, Pfau M, Sadda SR. Swept-Source OCT Angiography Imaging of the foveal avascular zone and macular capillary network density in diabetic retinopathy. Invest Ophthalmol Vis Sci. 2016;57:3907–13.CrossRef Al-Sheikh M, Akil H, Pfau M, Sadda SR. Swept-Source OCT Angiography Imaging of the foveal avascular zone and macular capillary network density in diabetic retinopathy. Invest Ophthalmol Vis Sci. 2016;57:3907–13.CrossRef
7.
go back to reference Freiberg FJ, Pfau M, Wons J, Wirth MA, Becker MD, Michels S. Optical coherence tomography angiography of the foveal avascular zone in diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol. 2016;254:1051–8.CrossRef Freiberg FJ, Pfau M, Wons J, Wirth MA, Becker MD, Michels S. Optical coherence tomography angiography of the foveal avascular zone in diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol. 2016;254:1051–8.CrossRef
8.
go back to reference Di G, Weihong Y, Xiao Z, Zhikun Y, Xuan Z, Yi Q, et al. A morphological study of the foveal avascular zone in patients with diabetes mellitus using optical coherence tomography angiography. Graefes Arch Clin Exp Ophthalmol. 2016;254:873–9.CrossRef Di G, Weihong Y, Xiao Z, Zhikun Y, Xuan Z, Yi Q, et al. A morphological study of the foveal avascular zone in patients with diabetes mellitus using optical coherence tomography angiography. Graefes Arch Clin Exp Ophthalmol. 2016;254:873–9.CrossRef
9.
go back to reference Simonett JM, Scarinci F, Picconi F, Giorno P, De Geronimo D, Di Renzo A, et al. Early microvascular retinal changes in optical coherence tomography angiography in patients with type 1 diabetes mellitus. Acta Ophthalmol. 2017;95:e751–5.CrossRef Simonett JM, Scarinci F, Picconi F, Giorno P, De Geronimo D, Di Renzo A, et al. Early microvascular retinal changes in optical coherence tomography angiography in patients with type 1 diabetes mellitus. Acta Ophthalmol. 2017;95:e751–5.CrossRef
10.
go back to reference Carnevali A, Sacconi R, Corbelli E, Tomasso L, Querques L, Zerbini G, et al. Optical coherence tomography angiography analysis of retinal vascular plexuses and choriocapillaris in patients with type 1 diabetes without diabetic retinopathy. Acta Diabetol. 2017;54:695–702.CrossRef Carnevali A, Sacconi R, Corbelli E, Tomasso L, Querques L, Zerbini G, et al. Optical coherence tomography angiography analysis of retinal vascular plexuses and choriocapillaris in patients with type 1 diabetes without diabetic retinopathy. Acta Diabetol. 2017;54:695–702.CrossRef
11.
go back to reference Gołębiewska J, Olechowski A, Wysocka-Mincewicz M, Odrobina D, Baszyńska-Wilk M, Groszek A, et al. Optical coherence tomography angiography vessel density in children with type 1 diabetes. PLoS One. 2017;12:e0186479.CrossRef Gołębiewska J, Olechowski A, Wysocka-Mincewicz M, Odrobina D, Baszyńska-Wilk M, Groszek A, et al. Optical coherence tomography angiography vessel density in children with type 1 diabetes. PLoS One. 2017;12:e0186479.CrossRef
12.
go back to reference Li T, Jia Y, Wang S, Wang A, Gao L, Yang C, Zou H. Retinal microvascular abnormalities in children with type 1 diabetes mellitus without visual impairment or diabetic retinopathy. Invest Ophthalmol Vis Sci. 2019;60:990–8.CrossRef Li T, Jia Y, Wang S, Wang A, Gao L, Yang C, Zou H. Retinal microvascular abnormalities in children with type 1 diabetes mellitus without visual impairment or diabetic retinopathy. Invest Ophthalmol Vis Sci. 2019;60:990–8.CrossRef
13.
go back to reference Inanc M, Tekin K, Kiziltoprak H, Ozalkak S, Doguizi S, Aycan Z. Changes in retinal microcirculation precede the clinical onset of diabetic retinopathy in children with type 1 diabetes mellitus. Am J Ophthalmol. 2019;1:19 (Epub ahead of print). Inanc M, Tekin K, Kiziltoprak H, Ozalkak S, Doguizi S, Aycan Z. Changes in retinal microcirculation precede the clinical onset of diabetic retinopathy in children with type 1 diabetes mellitus. Am J Ophthalmol. 2019;1:19 (Epub ahead of print).
14.
go back to reference Lupidi M, Coscas F, Cagini C, Fiore T, Spaccini E, Fruttini D, et al. Automated quantitative analysis of retinal microvasculature in normal eyes on optical coherence tomography angiography. Am J Ophthalmol. 2016;169:9–23.CrossRef Lupidi M, Coscas F, Cagini C, Fiore T, Spaccini E, Fruttini D, et al. Automated quantitative analysis of retinal microvasculature in normal eyes on optical coherence tomography angiography. Am J Ophthalmol. 2016;169:9–23.CrossRef
15.
go back to reference Abraham MB, Jones TW, Naranjo D, Karges B, Oduwole A, Tauschmann M, et al. ISPAD Clinical Practice Consensus Guidelines 2018: assessment and management of hypoglycemia in children and adolescents with diabetes. Pediatr Diabetes. 2018;19(Suppl 27):178–92.CrossRef Abraham MB, Jones TW, Naranjo D, Karges B, Oduwole A, Tauschmann M, et al. ISPAD Clinical Practice Consensus Guidelines 2018: assessment and management of hypoglycemia in children and adolescents with diabetes. Pediatr Diabetes. 2018;19(Suppl 27):178–92.CrossRef
16.
go back to reference Urakami T, Yoda M, Yoshida K, Mine Y, Aoki M, Suzuki J. Renal glucosuria in schoolchildren: clinical characteristics. Send to Pediatr Int. 2018;60:35–40.CrossRef Urakami T, Yoda M, Yoshida K, Mine Y, Aoki M, Suzuki J. Renal glucosuria in schoolchildren: clinical characteristics. Send to Pediatr Int. 2018;60:35–40.CrossRef
17.
go back to reference Takase N, Nozaki M, Kato A, Ozeki H, Yoshida M, Ogura Y. Ealuated by face optical coherence tomography angiography. Retina. 2015;35:2377–83.CrossRef Takase N, Nozaki M, Kato A, Ozeki H, Yoshida M, Ogura Y. Ealuated by face optical coherence tomography angiography. Retina. 2015;35:2377–83.CrossRef
18.
go back to reference McLeod DS, Lefer DJ, Merges C, Lutty GA. Enhanced expression of intracellular adhesion molecule-1 and P-selectin in the diabetic human retina and choroid. Am J Pathol. 1995;147:642–53.PubMedPubMedCentral McLeod DS, Lefer DJ, Merges C, Lutty GA. Enhanced expression of intracellular adhesion molecule-1 and P-selectin in the diabetic human retina and choroid. Am J Pathol. 1995;147:642–53.PubMedPubMedCentral
19.
go back to reference Miyamoto K, Khosrof S, Bursell SE, Rohan R, Murata T, Clermont AC, et al. Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition. Proc Natl Acad Sci USA. 1999;96:10836–41.CrossRef Miyamoto K, Khosrof S, Bursell SE, Rohan R, Murata T, Clermont AC, et al. Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition. Proc Natl Acad Sci USA. 1999;96:10836–41.CrossRef
20.
go back to reference Chibber R, Ben-Mahmud BM, Chibber S, Kohner EM. Leukocytes in diabetic retinopathy. Curr Diabetes Rev. 2007;3:3–14.CrossRef Chibber R, Ben-Mahmud BM, Chibber S, Kohner EM. Leukocytes in diabetic retinopathy. Curr Diabetes Rev. 2007;3:3–14.CrossRef
21.
go back to reference Liu Y, Shen J, Fortmann SD, Wang J, Vestweber D, Campochiaro PA. Reversible retinal vessel closure from VEGF-induced leukocyte plugging. JCI Insight. 2017;2:e95530.CrossRef Liu Y, Shen J, Fortmann SD, Wang J, Vestweber D, Campochiaro PA. Reversible retinal vessel closure from VEGF-induced leukocyte plugging. JCI Insight. 2017;2:e95530.CrossRef
22.
go back to reference Gruden G, Giunti G, Barutta F, Chaturvedi N, Witte DR, Tricarico M, et al. QTc Interval prolongation is independently associated with severe hypoglycemic attacks in type 1 diabetes from the EURODIAB IDDM complications study. Diabetes Care. 2012;35:125–7.CrossRef Gruden G, Giunti G, Barutta F, Chaturvedi N, Witte DR, Tricarico M, et al. QTc Interval prolongation is independently associated with severe hypoglycemic attacks in type 1 diabetes from the EURODIAB IDDM complications study. Diabetes Care. 2012;35:125–7.CrossRef
23.
go back to reference Kilpatrick ES, Rigby AS, Atkin SL, Frier BM. Does severe hypoglycaemia influence microvascular complications in Type 1 diabetes? An analysis of the Diabetes Control and Complications Trial database. Diabet Med. 2012;29:1195–8.CrossRef Kilpatrick ES, Rigby AS, Atkin SL, Frier BM. Does severe hypoglycaemia influence microvascular complications in Type 1 diabetes? An analysis of the Diabetes Control and Complications Trial database. Diabet Med. 2012;29:1195–8.CrossRef
24.
go back to reference Wright RJ, Frier BM. Vascular Disease and Diabetes: Is hypoglycaemia an aggravating factor? Diabetes Metab Res Rev. 2008;24:353–63.CrossRef Wright RJ, Frier BM. Vascular Disease and Diabetes: Is hypoglycaemia an aggravating factor? Diabetes Metab Res Rev. 2008;24:353–63.CrossRef
25.
go back to reference Kowluru RA, Kowluru A, Mishra M, Kumar B. Oxidative stress and epigenetic modifications in the pathogenesis of diabetic retinopathy. Prog Retin Eye Res. 2015;48:40–61.CrossRef Kowluru RA, Kowluru A, Mishra M, Kumar B. Oxidative stress and epigenetic modifications in the pathogenesis of diabetic retinopathy. Prog Retin Eye Res. 2015;48:40–61.CrossRef
Metadata
Title
Foveal avascular zone area analysis in juvenile-onset type 1 diabetes using optical coherence tomography angiography
Authors
Hajime Onoe
Yorihisa Kitagawa
Hiroyuki Shimada
Ari Shinojima
Masako Aoki
Tatsuhiko Urakami
Publication date
01-05-2020
Publisher
Springer Japan
Published in
Japanese Journal of Ophthalmology / Issue 3/2020
Print ISSN: 0021-5155
Electronic ISSN: 1613-2246
DOI
https://doi.org/10.1007/s10384-020-00726-3

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