Abstract
Purpose
The objective of this study was to evaluate the vascular parameters of the retinal zones and the optic disc (OD) with the use of optical coherence tomography angiography (OCTA) in pediatric patients with type 1 diabetes mellitus (T1DM).
Methods
This study enrolled 60 patients with T1DM without clinically detectable diabetic retinopathy (DR), along with 59 age-, gender-, and pubertal stage-matched controls. The ages of the participants in both groups were < 18 years. Retinal and OD measurements were carried out with OCTA. Foveal avascular zone (FAZ) area, non-flow area (NFA), FAZ perimeter (PERIM), acircularity index of FAZ (AI, the rate of the perimeter of FAZ and the perimeter of a circle with equal area), foveal density (FD), superficial (SCP), and the deep capillary plexus (DCP) were analyzed in the macular region. SCP and DCP were also scanned centered on the OD. Correlations between the OCTA parameters with duration of DM, glycated hemoglobin (HbA1c) levels, and microalbuminuria were evaluated among patients with T1DM.
Results
The mean values for NFA were significantly higher and mean FD were significantly lower in the diabetic group compared with the controls (p = 0.02 and p = 0.01, respectively). The mean values for SCP and DCP were significantly lower in diabetic group (p < 0.05). The mean values for capillary density in the OD were also significantly lower in diabetic group (p < 0.05). There were correlations between the duration of T1DM, HbA1c levels and microalbuminuria, and the investigated parameters of OCTA.
Conclusions
The presence of microvascular changes in both retinal zones and the OD in children with T1DM without retinopathy is an important data. OCTA can be used for the early detection of DR in children.
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References
Lueder GT, Silverstein J (2005) Screening for retinopathy in the pediatric patient with type 1 diabetes mellitus. Pediatrics 116(1):270–273
Maahs DM, Daniels SR, De Ferranti SD, Dichek HL, Flynn J, Goldstein BI et al (2014) Cardiovascular disease risk factors in youth with diabetes mellitus: a scientific statement from the American Heart Association. Circulation 130(17):1532–1558
Molitch ME, Steffes MW, Cleary PA, Nathan DM (1993) Baseline analysis of renal function in the diabetes control and complications trial. Kidney Int 43(3):668–674
Control D, Group CTR (1995) The relationship of glycemic exposure (HbA1c) to the risk of development and progression of retinopathy in the diabetes control and complications trial. Diabetes 44(8):968–983
Control D, Group CTR (1993) The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 329(14):977–986
Mameli C, Invernizzi A, Bolchini A, Bedogni G, Giani E, Macedoni M, Zuccotti G, Preziosa C, Pellegrini M (2019) Analysis of retinal perfusion in children, adolescents, and young adults with type 1 diabetes using optical coherence tomography angiography. J Diabetes Res. https://doi.org/10.1155/2019/5410672
Forlenza GP, Stewart MW (2012) Diabetic retinopathy in children. Pediatr Endocrinol Rev 10(2):217–226
Sultan MB, Starita C, Huang K (2012) Epidemiology, risk factors and management of paediatric diabetic retinopathy. Br J Ophthalmol 96(3):312–317
Graves LE, Donaghue KC (2019) Management of diabetes complications in youth. Ther Adv Endocrinol Metab 10:2042018819863226
Donaghue KC, Marcovecchio ML, Wadwa RP, Chew EY, Wong TY, Calliari LE, Zabeen B, Salem MA, Craig ME (2018) ISPAD Clinical Practice Consensus Guidelines 2018: microvascular and macrovascular complications in children and adolescents. Pediatr Diabetes 27(19):262–274
Koller H, Fierson W, Trese M, Buckley E, Ellis GS Jr, Gross R et al (1998) Screening for retinopathy in the pediatric patient with type 1 diabetes mellitus. Pediatrics 101(2):313–314
Liew G, Wong VW, Ho I-V (2017) Mini review: changes in the incidence of and progression to proliferative and sight-threatening diabetic retinopathy over the last 30 years. Ophthalmic Epidemiol 24(2):73–80
Scanlon PH, Stratton IM, Bachmann MO, Jones C, Leese GP, Four Nations Diabetic Retinopathy Screening Study G (2016) Risk of diabetic retinopathy at first screen in children at 12 and 13 years of age. Diabet Med 33(12):1655–1658
Simonett JM, Scarinci F, Picconi F, Giorno P, De Geronimo D, Di Renzo A, Varano M, Frontoni S, Parravano M (2017) Early microvascular retinal changes in optical coherence tomography angiography in patients with type 1 diabetes mellitus. Acta Ophthalmol 95(8):e751–e755
De Carlo TE, Romano A, Waheed NK, Duker JS (2015) A review of optical coherence tomography angiography (OCTA). Int J Retina Vitreous 1(1):5
Inanc M, Tekin K, Kiziltoprak H, Ozalkak S, Doguizi S, Aycan Z (2019) Changes in retinal microcirculation precede the clinical onset of diabetic retinopathy in children with type 1 diabetes mellitus. Am J Ophthalmol 207:37–44
Tanner JM, Whitehouse RH (1976) Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty. Arch Dis Child 51(3):170–179
Lurbe E, Cifkova R, Cruickshank JK, Dillon MJ, Ferreira I, Invitti C et al (2009) Management of high blood pressure in children and adolescents: recommendations of the European Society of Hypertension. J Hypertens 27(9):1719–1742
Sandhu HS, Elmogy M, El-Adawy N, Eltanboly A, Shalaby A, Keynton R, El-Baz A (2020) Automated diagnosis of diabetic retinopathy using clinical biomarkers, optical coherence tomography (OCT), and OCT angiography. Am J Ophthalmol. https://doi.org/10.1016/j.ajo.2020.01.016
Arend O, Wolf S, Harris A, Reim M (1995) The relationship of macular microcirculation to visual acuity in diabetic patients. Arch Ophthalmol 113(5):610–614
Onoe H, Kitagawa Y, Shimada H, Shinojima A, Aoki M, Urakami T (2020) Foveal avascular zone area analysis in juvenile-onset type 1 diabetes using optical coherence tomography angiography. Jpn J Ophthalmol. https://doi.org/10.1007/s10384-020-00726-3
Gołębiewska J, Olechowski A, Wysocka-Mincewicz M, Odrobina D, Baszyńska-Wilk M, Groszek A, Szalecki M, Hautz W (2017) Optical coherence tomography angiography vessel density in children with type 1 diabetes. PLoS One 12(10):e0186479
Carnevali A, Sacconi R, Corbelli E, Tomasso L, Querques L, Zerbini G, Scorcia V, Bandello F, Querques G (2017) Optical coherence tomography angiography analysis of retinal vascular plexuses and choriocapillaris in patients with type 1 diabetes without diabetic retinopathy. Acta Diabetol 54(7):695–702
Andreasson R, Ekelund C, Landin-Olsson M, Nilsson C (2018) HbA1c levels in children with type 1 diabetes and correlation to diabetic retinopathy. J Pediatr Endocrinol Metab 31(4):369–374
Klein R, Klein BE, Moss SE, Davis MD, DeMets DL (1984) The Wisconsin Epidemiologic Study of Diabetic Retinopathy: II. Prevalence and risk of diabetic retinopathy when age at diagnosis is less than 30 years. Arch Ophthalmol 102(4):520–526
Jeganathan VS, Wang JJ, Wong TY (2008) Ocular associations of diabetes other than diabetic retinopathy. Diabetes Care 31(9):1905–1912
Newman NJ, Dickersin K, Kaufman D, Kelman S, Scherer R (1996) Characteristics of patients with nonarteritic anterior ischemic optic neuropathy eligible for the ischemic optic neuropathy decompression trial. Arch Ophthalmol 114(11):1366–1374
Piltz-seymour JR, Grunwald JE, Hariprasad SM, Dupont J (2001) Optic nerve blood flow is diminished in eyes of primary open-angle glaucoma suspects. Am J Ophthalmol 132(1):63–69
Flammer J, Orgul S, Costa VP, Orzalesi N, Krieglstein GK, Serra LM, Renard JP, Stefansson E (2002) The impact of ocular blood flow in glaucoma. Prog Retin Eye Res 21(4):359–393
Barr CC, Glaser JS, Blankenship G (1980) Acute disc swelling in juvenile diabetes. Clinical profile and natural history of 12 cases. Arch Ophthalmol 98(12):2185–2192
Bandello F, Menchini F (2004) Diabetic papillopathy as a risk factor for progression of diabetic retinopathy. Retina 24(1):183–184
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Concept: Ozlem Kara, Mehmet Erol Can
Design: Ozlem Kara, Mehmet Erol Can
Definition of intellectual content: Ozlem Kara, Mehmet Erol Can
Literature Search: Ozlem Kara, Mehmet Erol Can
Data acquisition: Ozlem Kara, Mehmet Erol Can
Data analysis: Ozlem Kara, Mehmet Erol Can
Statistical analysis: Ozlem Kara, Mehmet Erol Can
Manuscript preparation: Ozlem Kara, Mehmet Erol Can
Manuscript editing and manuscript review: Ozlem Kara, Mehmet Erol Can
The guarantors of manuscript are Ozlem Kara and Mehmet Erol Can
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The manuscript was presented as an oral presentation in the Turkish Ophthalmological Association 16th March Symposium in Erzurum, Turkey at March 15-17, 2019
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Kara, O., Can, M.E. Evaluation of microvascular changes in retinal zones and optic disc in pediatric patients with type 1 diabetes mellitus. Graefes Arch Clin Exp Ophthalmol 259, 323–334 (2021). https://doi.org/10.1007/s00417-020-04935-x
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DOI: https://doi.org/10.1007/s00417-020-04935-x