Evaluation of early retinal vascular changes by optical coherence tomography angiography in children with type 1 diabetes mellitus without diabetic retinopathy.


Journal

International ophthalmology
ISSN: 1573-2630
Titre abrégé: Int Ophthalmol
Pays: Netherlands
ID NLM: 7904294

Informations de publication

Date de publication:
Feb 2022
Historique:
received: 24 04 2021
accepted: 21 09 2021
pubmed: 10 10 2021
medline: 3 3 2022
entrez: 9 10 2021
Statut: ppublish

Résumé

To evaluate macular and peripapillary vascular changes by optical coherence tomography angiography (OCTA) in children with type 1 diabetes mellitus (T1DM) without diabetic retinopathy (DR). This study included 46 patients with T1DM and 46 age-sex matched healthy subjects. All participants were evaluated in terms of macular and optic disk parameters by using AngioVue. Foveal avascular zone (FAZ) area, macular and optic disk vessel density (VD) were analyzed. The correlation of these parameters with metabolic factors such as disease duration, mean hemoglobin A1c (HbA1c), insulin-like growth factor 1 (IGF-1) standard deviation score (SDS), homocysteine (Hcy) level, body mass index (BMI) SDS and daily insulin dose was also investigated in T1DM group. No significant difference was found in FAZ area and optic disk radial peripapillary capillary (RPC) VD comparing diabetic and control groups. In all macular regions, VD was significantly lower in T1DM versus control group both in superficial capillary plexus (SCP) and deep capillary plexus (DCP). None of the metabolic parameters was correlated with FAZ area and optic disk RPC-VD. Vascular density in SCP was negatively correlated with mean HbA1c and positively correlated with IGF-1 SDS. Homocysteine level was negatively correlated with DCP-VD in all areas. In children with T1DM without clinically apparent DR, VD in SCP and DCP was decreased and OCTA is a valuable imaging technique for detecting early vascular changes. The metabolic parameters such as mean HbA1c, IGF-1 SDS and Hcy affect the macular VD in diabetic children. 2011-KAEK-2, 2021/4, Trial registration date: 02.04.2021.

Identifiants

pubmed: 34625889
doi: 10.1007/s10792-021-02059-7
pii: 10.1007/s10792-021-02059-7
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

423-433

Informations de copyright

© 2021. The Author(s), under exclusive licence to Springer Nature B.V.

Références

World Health Organisation (2006) Definition and diagnosis of diabetes mellitus and intermediate hyperglycaemia: report of a WHO/IDF consultation. Switzerland, Geneva
American Diabetes Association (2014) Standards of medical care in diabetes. Diabetes Care 37:S14–S80
doi: 10.2337/dc14-S014
Mobasseri M, Shirmohammadi M, Amiri T, Vahed N, Hosseini Fard H, Ghojazadeh M (2020) Prevalence and incidence of type 1 diabetes in the world: a systematic review and meta-analysis. Health Promot Perspect 10(2):98–115. https://doi.org/10.34172/hpp.2020.18 .
IDF Diabetes Atlas (2017) 8th edn. Brussels, Belgium: International Diabetes Federation.
Mayer-Davis EJ, Kahkoska AR, Jefferies C, Dabelea D, Balde N, Gong CX, Aschner P, Craig ME (2018) ISPAD Clinical Practice Consensus Guidelines 2018: definition, epidemiology, and classification of diabetes in children and adolescents. Pediatr Diabetes 19(Suppl 27):7–19. https://doi.org/10.1111/pedi.12773
doi: 10.1111/pedi.12773 pubmed: 30226024 pmcid: 7521365
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 19(Suppl 27):262–274. https://doi.org/10.1111/pedi.12742
doi: 10.1111/pedi.12742 pubmed: 30079595 pmcid: 8559793
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
doi: 10.1007/s00592-017-0996-8
Demir ST, Ucar A, Elitok GK, Karatas ME, Karapapak M, Kutucu OK, Uzun SU, Guven D (2020) Evaluation of retinal neurovascular structures by optical coherence tomography and optical coherence tomography angiography in children and adolescents with type 1 diabetes mellitus without clinical sign of diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 258(11):2363–2372
doi: 10.1007/s00417-020-04842-1
Chen YJ, Khouri AS, Zarbin MA, Szirth BC (2020) Early retinal microvascular abnormalities in young adults with Type 1 diabetes mellitus without clinically evident diabetic retinopathy. Retina. https://doi.org/10.1097/IAE.0000000000003047
doi: 10.1097/IAE.0000000000003047 pubmed: 33217618 pmcid: 7889285
Li T, Jia Y, Wang S, Wang A, Gao L, Yang C, Zou H (2019) Retinal microvascular abnormalities in children with Type 1 diabetes mellitus without visual impairment or diabetic retinopathy. Invest Ophthalmol Vis Sci 60(4):990–998. https://doi.org/10.1167/iovs.18-25499 .
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 8(2019):5410672. https://doi.org/10.1155/2019/5410672
doi: 10.1155/2019/5410672
Watkins RA, Evans-Molina C, Blum JS, Dimeglio LA (2014) Established and emerging biomarkers for the prediction of type 1 diabetes: a systematic review. Transl Res 164:110–121
doi: 10.1016/j.trsl.2014.02.004
Demir K, Özen S, Konakçı E, Aydın M, Darendeliler F (2017) A Comprehensive Online Calculator for Pediatric Endocrinologists: ÇEDD Çözüm/TPEDS Metrics. J Clin Res Pediatr Endocrinol 9:182–184
doi: 10.4274/jcrpe.4526
Guven B, Can M, Mungan G, Acikgoz S (2013) Reference values for serum levels of insulin-like growth factor 1 (IGF-1) and IGF-binding protein 3 (IGFBP-3) in the West Black Sea region of Turkey. Scand J Clin Lab Invest 73(2):135–140
doi: 10.3109/00365513.2012.755739
Takase N, Nozaki M, Kato A, Ozeki H, Yoshida M, Ogura Y (2015) Enlargement of foveal avascular zone in diabetic eyes evaluated by en face optical coherence tomography angiography. Retina 35:2377–2383 https://doi.org/10.1097/IAE.0000000000000849 .
Mansour AM, Schachat A, Bodiford G, Haymond R (1993) Foveal avascular zone in diabetes mellitus. Retina 13:125–128.
Niestrata-Ortiz M, Fichna P, Stankiewicz W, Stopa M (2019) Enlargement of the foveal avascular zone detected by optical coherence tomography angiography in diabetic children without diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 257(4):689–697. https://doi.org/10.1007/s00417-019-04264-8
doi: 10.1007/s00417-019-04264-8 pubmed: 30824996
Kara O, Erol Can M (2021) Evaluation of microvascular changes in retinal zones and optic disc in pediatric patients with type 1 diabetes mellitus. Graefes Arch Clin Exp Ophthalmol 259(2):323–334. https://doi.org/10.1007/s00417-020-04935-x .
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. https://doi.org/10.1016/j.ajo.2019.04.011
doi: 10.1016/j.ajo.2019.04.011 pubmed: 31009594
Vujosevic S, Muraca A, Alkabes M, Villani E, Cavarzeran F, Rossetti L, De Cillaʼ S (2019) Early microvascular and neural changes in patients with type 1 and type 2 diabetes mellitus without clinical signs of diabetic retinopathy. Retina 39(3):435–445. https://doi.org/10.1097/IAE.0000000000001990
doi: 10.1097/IAE.0000000000001990 pubmed: 29206758
Scarinci F, Picconi F, Virgili G, Varano M, Giorno P, Frontoni S, Parravano M (2020) Microvascular impairment as a biomarker of diabetic retinopathy progression in the long-term follow up in type 1 diabetes. Sci Rep 10(1):18266. https://doi.org/10.1038/s41598-020-75416-8
doi: 10.1038/s41598-020-75416-8 pubmed: 33106539 pmcid: 7589477
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. https://doi.org/10.1111/aos.13404
doi: 10.1111/aos.13404 pubmed: 28211261
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. https://doi.org/10.1371/journal.pone.0186479
doi: 10.1371/journal.pone.0186479 pubmed: 29053718 pmcid: 5650189
Spencer BG, Estevez JJ, Liu E, Craig JE, Finnie JW (2020) Pericytes, inflammation, and diabetic retinopathy. Inflammopharmacology 28(3):697–709. https://doi.org/10.1007/s10787-019-00647-9
doi: 10.1007/s10787-019-00647-9 pubmed: 31612299
Gardner TW, Davila JR (2017) The neurovascular unit and the pathophysiologic basis of diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 255(1):1–6. https://doi.org/10.1007/s00417-016-3548-y
doi: 10.1007/s00417-016-3548-y pubmed: 27832340
Forlenza GP, Stewart MW (2013) Diabetic retinopathy in children. Pediatr Endocrinol Rev 10:217–226.
Vujosevic S, Muraca A, Gatti V, Masoero L, Brambilla M, Cannillo B, Villani E, Nucci P, De Cillà S (2018) Peripapillary microvascular and neural changes in diabetes mellitus: an OCT-Angiography Study. Invest Ophthalmol Vis Sci 59(12):5074–5081. https://doi.org/10.1167/iovs.18-24891
doi: 10.1167/iovs.18-24891 pubmed: 30357402
Amin R, Widmer B, Prevost AT et al (2008) Risk of microalbuminuria and progression to macroalbuminuria in a cohort with childhood onset type 1 diabetes: prospective observational study. BMJ 336:697–701
doi: 10.1136/bmj.39478.378241.BE
Benitez-Aguirre P, Craig ME, Cass HG, Sugden CJ, Jenkins AJ, Wang JJ, Cusumano J, Hodgson LAB, Lee K, Wong TY, Donaghue KC (2014) Sex differences in retinal microvasculature through puberty in type 1 diabetes: are girls at greater risk of diabetic microvascular complications? Invest Ophthalmol Vis Sci 56(1):571–577. https://doi.org/10.1167/iovs.14-15147
doi: 10.1167/iovs.14-15147 pubmed: 25477322
Marcovecchio ML, Dalton RN, Schwarze CP, Prevost AT, Neil HAW, Acerini CL, Barrett T, Cooper JD, Edge J, Shield J, Widmer B, Todd JA, Dunger DB (2009) Ambulatory blood pressure measurements are related to albumin excretion and are predictive for risk of microalbuminuria in young people with type 1 diabetes. Diabetologia 52:1173–1181. https://doi.org/10.1007/s00125-009-1327-6
doi: 10.1007/s00125-009-1327-6 pubmed: 19305965
Gallego PH, Craig ME, Hing S, Donaghue KC (2008) Role of blood pressure in development of early retinopathy in adolescents with type 1 diabetes: prospective cohort study. BMJ 337:a918–a918
doi: 10.1136/bmj.a918
Loredana Marcovecchio M, Neil Dalton R, Toby Prevost A, Acerini CL, Barrett TG, Cooper JD, Edge J, Neil A, Shield J, Widmer B, Todd JA, Dunger DB (2009) Prevalence of abnormal lipid profiles and the relationship with the development of microalbuminuria in adolescents with type 1 diabetes. Diabetes Care 32:658–663. https://doi.org/10.2337/dc08-1641
doi: 10.2337/dc08-1641 pubmed: 19171721
Raile K, Galler A, Hofer S, Herbst A, Dunstheimer D, Busch P, Holl RW (2007) Diabetic nephropathy in 27,805 children, adolescents, and adults with type 1 diabetes: effect of diabetes duration, A1C, hypertension, dyslipidemia, diabetes onset, and sex. Diabetes Care 30:2523–2528. https://doi.org/10.2337/dc07-0282
doi: 10.2337/dc07-0282 pubmed: 17630266
Jenkins AJ, Lyons TJ, Zheng D, Otvos JD, Lackland DT, McGee D, Garvey WT, Klein RL; DCCT/EDIC Research Group (2003) Lipoproteins in the DCCT/EDIC cohort: associations with diabetic nephropathy. Kidney Int 64(3):817–28. https://doi.org/10.1046/j.1523-1755.2003.00164.x .
Wilkinson-Berka JL, Wraight C, Werther G (2006) The role of growth hormone, insulin-like growth factor and somatostatin in diabetic retinopathy. Curr Med Chem 13(27):3307–3317. https://doi.org/10.2174/092986706778773086
doi: 10.2174/092986706778773086 pubmed: 17168853
Raman P, Singal AK, Behl A (2019) Effect of insulin-like Growth Factor-1 on diabetic retinopathy in pubertal age patients with Type 1 diabetes. Asia Pac J Ophthalmol (Phila) 8(4):319–323. https://doi.org/10.1097/APO.0000000000000250 .
Meng S, Ciment S, Jan M, Tran T, Pham H, Cueto R, Yang XF, Wang H (2013) Homocysteine induces inflammatory transcriptional signaling in monocytes. Front Biosci (Landmark Ed) 1(18):685–695. https://doi.org/10.2741/4131
doi: 10.2741/4131
Hayden MR, Tyagi SC (2004) Homocysteine and reactive oxygen species in metabolic syndrome, type 2 diabetes mellitus, and atheroscleropathy: the pleiotropic effects of folate supplementation. Nutr J 10(3):4. https://doi.org/10.1186/1475-2891-3-4
doi: 10.1186/1475-2891-3-4
Poddar R, Sivasubramanian N, DiBello PM, Robinson K, Jacobsen DW (2001) Homocysteine induces expression and secretion of monocyte chemoattractant protein-1 and interleukin-8 in human aortic endothelial cells: implications for vascular disease. Circulation 103(22):2717–2723. https://doi.org/10.1161/01.cir.103.22.2717
doi: 10.1161/01.cir.103.22.2717 pubmed: 11390343
Wierzbicki AS (2007) Homocysteine and cardiovascular disease: a review of the evidence. Diab Vasc Dis Res 4(2):143–150. https://doi.org/10.3132/dvdr.2007.033
doi: 10.3132/dvdr.2007.033 pubmed: 17654449
Tawfik A, Mohamed R, Elsherbiny NM, DeAngelis MM, Bartoli M, Al-Shabrawey M (2019)Homocysteine: a potential biomarker for diabetic retinopathy. J Clin Med 8(1):121. https://doi.org/10.3390/jcm8010121
doi: 10.3390/jcm8010121 pmcid: 6352029
Feng Y, Shan MQ, Bo L, Zhang XY, Hu J (2015) Association of homocysteine with type 1 diabetes mellitus: a meta-analysis. Int J Clin Exp Med 8(8):12529–12538
pubmed: 26550163 pmcid: 4612848
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 64(3):271–277. https://doi.org/10.1007/s10384-020-00726-3
doi: 10.1007/s10384-020-00726-3 pubmed: 32125552
Wysocka-Mincewicz M, Baszyńska-Wilk M, Gołębiewska J, Andrzej Olechowski A, Byczyńska A, Hautz W, Szalecki M (2020) Influence of metabolic parameters and treatment method on OCT angiography results in children with Type 1 diabetes. J Diabetes Res 2020:4742952. https://doi.org/10.1155/2020/4742952
doi: 10.1155/2020/4742952 pubmed: 33294460 pmcid: 7688367

Auteurs

Serkan Bilge Koca (SB)

Faculty of Medicine, Department of Pediatrics, Division of Pediatric Endocrinology, Afyonkarahisar Health Sciences University, Afyonkarahisar, Turkey.

Muberra Akdogan (M)

Faculty of Medicine, Department of Ophthalmology, Afyonkarahisar Health Sciences University, Afyonkarahisar, Turkey.

Semra Koca (S)

Faculty of Medicine, Department of Ophthalmology, Afyonkarahisar Health Sciences University, Afyonkarahisar, Turkey. drsemrakara68@hotmail.com.
, 1444. Sokak Kandilli Konakları D Blok 2/8, Afyonkarahisar, Türkiye. drsemrakara68@hotmail.com.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH