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PRE-RETINOPATHY OF TYPE 1 DIABETES IN THE CONTEXT OF FUNCTIONAL, STRUCTURAL AND MICROCIRCULATORY CHANGES IN THE MACULAR AREA


Authors: J. Krásný;  L. Magera;  P. Pluhovský;  J. Čeledová;  L. Holubová
Authors‘ workplace: Oční klinika Fakultní nemocnice Královské Vinohrady v Praze
Published in: Čes. a slov. Oftal., 77, 2021, No. 4, p. 170-182
Category: Original Article
doi: https://doi.org/10.31348/2021/20

Overview

Aim: The authors assessed the development of intraocular changes in type 1 diabetes (T1DM) from the onset of the disease leading to diabetic retinopathy (DR). The quote: “There must be an intermediate stage between the physiological intraocular finding and the diabetic retinopathy itself “, (prof. Jan Vavřinec).

Methods: A two-year study (2018 and 2019) was conducted at the Department of Ophthalmology of the Teaching Hospital Kralovske Vinohrady in Prague (Czech Republic). There were 54 patients aged 17–42 years, the detection of T1DM ranged between the 1st and 14th year of life, with a duration of 12–35 years. Individual patients were always examined simultaneously by three methods: CS (contrast sensitivity), SD-OCT (spectral domain optical coherence tomography) and OCT-A (optical coherence tomography-angiography). We examined 106 eyes once and in a comprehensive manner.

Results: We have shown that there is an intermediate stage between the physiological finding on the retina and DR, so-called diabetic pre-retinopathy (DpR). Subsequent redistribution of the observed into two DpR subgroups was derived from the size of the FAZ, either with its smaller area or with a larger area determining the microvascularity of the central area of the retina. The results of both other methods were assigned to these values. For SD-OCT, the depth of the fovea (the difference between the central retinal thickness and the total average retinal thickness) was determined, which was affected by the increased the macular cubature. In all patients it was on average 10.3 μm3. The retina in the central area was significantly strengthened compared to the healthy population at the level of significance p ≤ 0,001. We divided the actual DpR into an image: DpR1 in 26.5 % of eyes – condition with an average shallower fovea only by 21.5 μm below the level of the surrounding retina and an average narrower FAZ: 0.165 mm2 and with a more significant decrease in CS; DpR2 in 40.5 % of eyes – condition with average deeper fovea by 42 μm, i.e., more significantly and average larger FAZ: 0.325 mm2 with lower decrease of CS. At the same time, other changes in microvascularity were noted, such as disorders in the sense of non-perfusion in the central part of the retina of various degrees. This finding differed significantly from changes in already established (non-proliferative) NPDR in 36 % of eyes, when a significant decrease in CS with normal visual acuity was found 4/4 ETDRS. Statistical differences in CS between DpR1 and DpR2 and NPDR were determined – always p ≤ 0.001. The average depth of the fovea was NPDR: 29.5 μm. NPDR had the largest average FAZ: 0.56 mm2. Also significant were the most significant changes in non-perfusion and especially the presence of microaneurysms.

Conclusions: These three non - invasive methods helped to monitor the dynamics of the development of ocular changes in T1DM of better quality than the determination of visual acuity and ophthalmoscopic examination. Increased retinal volume induced hypoxia of visual cells with subsequent dual autoregulatory mechanism conditioning two types of diabetic pre-retinopathy before the onset of DR.

Keywords:

contrast sensitivity – Diabetic retinopathy – OCT-A – SD-OCT – T1DM


Sources
  1. Cunha-Vaz JG. Pathophysiology of diabetic retinopathy. Br J Ophthalmol.1978;62(6):351-355.
  2. Cunha-Vaz JG, Goldberg MF, Vygantas C, Noth J. Early detection of retinal involvement in diabetes by vitreous fluorophotometry. Ophthalmology. 1979;86(2):264-275.
  3. Sosna T, Bouček T, Fišer I. Diabetická retinopatie [Diabetic retinopathy], 1. vyd. Praha (Česká republika); Jiří Cendelín; 2001. 255. Czech.
  4. Kalvodová B, Sosna T, Ernest J, at al. Doporučené postupy pro diagnostiku a léčbu diabetické retinopatie [Recommended procedures for the diagnosis and treatment of diabetic retinopathy]. Ces Slov Oftal. 2016;76(6):226-233. Czech.
  5. Filouš A, Rychnová J, Vavřinec J.: Rozšířená klasifikace diabetické retinopatie u dětí a mladistvých [Extended clessification of diabetic retinopathy in children and adolescents]. Cesk Pediatr. 1992;47(8):453-455. Czech.
  6. Klement UM, Freyler H.: Diabetic pre-retinopathy. Klin Mbl Augenheilk. 1980;176(2):313-316. German.
  7. Krásný J, Brunnerová R, Průhová Š, et. al. Test citlivosti na kontrast v časné detekci očních změn u dětí, dospívajících a mladých dospělých s diabetes mellitus I. typu [The contrast sensitivity test in early detection of ocular changes in the relation to the type 1 diabetes mellitus compensation in children, teenegers, and youg adults]. Cesk Slov Oftal. 2006;62(6):381-392. Czech.
  8. Verougstraete C, Tousweint D, De Schepper Z, Haehtjens M, Dorchy H. First microangiografic abnormalities in childhood diabetes – types of lesions. Graef´Arch Clin Exp Ophthal. 1991;229(1):24-32.
  9. Krásný J, Anděl M, Brunnerová R, et al. The contrast sensitivity test in early detection of ocular changes in the relation to the type 1 diabetes mellitus compensation in children, teenegers, and young adults. Recent Pat Inflamm Alergy Drug Discov. 2007;1(3):232-236.
  10. Krásný J, Vosáhlo J, Čeledová J, Hora I, Magera L, Veith M. Preretinopatie u mladistvých s diabetem 1. typu z pohledu vyšetření citlivosti na kontrast a koherenční tomografie [Contrast sensitivity and optic coherence tomography examinations in adolescent patients with diabetes mellitus type I preretinopathy (a pilot study)]. Cesk Slov Oftal. 2014; 70(4):123-130. Czech.
  11. Magera L, Krásný J, Pluhovský P, Holubová L. Foveal avaskular zone and macular microvasculature changes by OCT-Angiography in young pacients with type 1 diabetes (pilot study) Cesk Slov Oftal. 2020;76(4):111. doi:10.31348/2020/19
  12. Krásný J. Multidiciplinární využití citlivosti na kontrast [Multidisciplinary use of contrast sensitivity]. Cas Lek Ces. 2006;145(11):865-869. Czech.
  13. www. vectorvision.com /html/educationCSV1000norms.html
  14. Kolář P, et al. Věkem podmíněná okulární degenerace [Age-related macular degeneratin]. 1st ed. Praha: Grada Publishing; 2008. 148. Czech.
  15. Krásný J. Závěrečná zpráva výzkumného projektu MZ ČR IGA NR/7952-3 [Final report of the research project of the Ministry of health of the Czech Republic IGA NR/7952-3] Czech. MZ ČR, 2006.
  16. Wolf S, Wolf-Schnurrbusch U. Spectral-domain optical coherente tomography use in macular diseases: a review. Ophthalmologica. 2010;224(6):333-340.
  17. Němec P. Trendy soudobé oftalmologie (ed. Rozsíval P.), svazek 10, Praha (Czech Republic): Galén; 2017. OCT angiografie [OCT-angiographia] Czech; 33-55.
  18. Patterson ChC, Dahlquist GG, Gyürüs E, Green A, Soltész G; EURODIAB Study Group. Incidence trend for childhood type 1 diabetes in Europe during 1989-2003 and predicted new cases 2005-2020: multicentre prospective registration study. Lancet. 2009;373(9680):2027-2033.
  19. Cinek O, Kulich M, Sumik Z. The incidence of type 1 diabetes in young Czech children stopped rising. Pediatric Diabetes. 2012;13:559. doi: 10.1111lj.1399-5448.2012.00858x
  20. Patterson ChC, Harjutsalo V, Green A. Trends and cyclical variotion in the incidence of childhood type 1 diabetes in 26 Europen centres in the 25 years period 1989-2013: a multicentre progresive registration study, Diabetologica. 2019;62(6):408-417.
  21. DeBuc D, Gerding H, Cambera B, Somfai GM. The use optical koherence tomography foor the detection of early diabetic retinopathy. Klin Monbl Augenheilkd. 2018; 235(4):377-384.
  22. van Dijk HW, Kok PH, Garvin M, et al. Selective loss of inner retinal thickness in type 1 diabetic patients with minimal diabetic retinopathy. Invest Ophthal Vis Sci. 2009;50(7):3404-3409.
  23. Vujosevic S, Midena E. Retinal layer changes in human preclinic and early clinical diabetic retinopathy support early retinal and Müller cells alteration. J Diabetes Res. 2013; Jun 2013, doi: 101155/2013/90550058
  24. Asefzadeh B, Fich BM, Paramteau CE, Cavallareno AA. Macular thickness and systemic markers for diabetes in individual with no or mild diabetic retinopathy. Clin Experiment Ophthamol. 2008;36(5):455-463.
  25. DeBuc CD, Somfai GM, Ranganethon S, Tátrai E, Ferencz M, Puliafito CA. Reliability and reproducibility of macular segmentation using custom-built optical coherence tomography retrinal image analysis software. J Biomed Opt 2009;14(6 ). doi: 10.1117/1.3268773
  26. Toprak I, Frnkci SM, Yaylali GF, Marti C, Yaylali V. Early retinal neurodegeneration in preclinical diabetic retinopathy: a multifactorial investigetion. Eye (London). 2020;34(6):1100-1107.
  27. Vilarroel M, Ciudim A, Hermándes C, Simo R. Neurodegeneration: an early event of diabetic retinopathy. Word J Diabetes. 2010; May 2010, doi: 104339/Wi.v1.1257.
  28. Georgakopoulos CD, Elliopoulou MI. Exarchou AM, Tzimis V, Pharmamakakis NM, Spoiliotis BE. Decreased contrast sensitivity in children and adolescents with type 1 diabetes mellitus. J Pediatr Ophthalmol Strabismus. 2011;48(2):92-97.
  29. Kawasaki K, Yonemura K, Yokogawa Y, Saito N, Kawakita S. Correlation between EREG oscillatory potential psychophysical contrast sensitivity in diabetes. Doc Ophthalmol. 1986;64(2):209-215.
  30. Lopes de Faria JM, Katsumi O, Cagliero E, Nathan D, Hirosa T. Neurovcisual abnormalities preceding the retinopatrhyin púatients with long term type 1. diabetes mellitus. Graf Arch Clin Exp Ophthalmol. 2001;239(9):643-648.
  31. Martinelli V, Lacerenza M, Merenda M, Meschi F, Somazzi L. The objective assessment of visual contrast sensitivity by pattern reversal visual evoked potential in diabetes. J Diabet Complications 1988;2(1):44-46.
  32. Krill AE, Deutman HS. The varios categories of juvenile macular degeneration. Trans Am Ophtalmol Soc. 1972;70(3):220-245.
  33. Sokol S, Moskowitz A, Skarf B, Evans R, Molitch M, Senior B. Contrast sensitivity in diabetics with and without background retinopathy. Arch Ophthalmol. 1985;103(1):51-54.
  34. Della Sala S, Bertoni G, Somazzi L, Stubbe F, Wilkins AJ. Impaired contrast sensitivity in diabetic patients with and without retinopathy: a new technique for rapid assessment. Br J Ophthamol. 1985;69(2):136-142.
  35. Verrotti A, Lobefalo L, Petitti MT, et. Al. Relkationship between contraqst sensitivity and metabolit kontrola in diabetic with and without retinopathy. Ann Med. 1999;30(4):369-374.
  36. Bangstad HJ, Brochmann-Hansen O, Hultgren S, Dahl-Jorgensen K, Hanssen KF. Impaired contrast sensitivity in adolescents and young type 1 diabetic patients with microalbuminuria. Acta Ophthalmol. 1994;72(6):668-673.
  37. Mangouritaqs G, Katoulis E, Kepaptsoglou O, Zoupas C. Effect of induced hyperglycemia on contrast sensitivity function in insulin-dependent diabetioc patients. Ophthalmologe. 1995;92(2):142-147. German.
  38. Ewing FM, Deary IJ, McCrimmon RJ, Strachan MW, Frier BM. Effect of acute hypoglacemia on visual information processing in adults with type 1 diabetes mellitus. Physiol. Behav. 1998;64(5):653-660.
  39. Urban B, Bakunowicz-Lazarcyk A, Peczynska J, Urban M. The evaluation of contrast sensitivity in children and adolescents with insulin-dependent diabetes mellitus. Klin Oczna. 1999;101(2):111-114. Polish.
  40. North RV, Farrell U, Banford D, et asl. Visual fiction in young IDDM patiens over 8 years of age. A 4year longitudinal study. Diabetes Care. 1997;20(11):1724-1730.
  41. Bancroft D, North RV, Dolben J, Butler G, Owens DR. Longitudinal study of viosual functions in young insulin dependent diabetics. Ophtalmic Physiol Opt. 1994;14(4):339-346.
  42. Liska V, Dostalek M. Are contrast sensitivity functions impared in insulin dependent diabetics without diabetic retinopathy? Acta Medica (Hradec Kralove) 1999;42(4):133-138.
  43. Liska V. Funkce kontrastní citlivosti u diabetes 1. typu (IDDM) bez příznaků diabetické retinopatie [Function of contrast sensitivity in diabetics type 1 (IDDM) without sings diabetic retinopathy]. Cesk Oftal. 1999;55(4):237-245. Czech.
  44. Katz G, Levkovitch-Verbin H, Treister G, Belkin M, Ilany J, Polat U. Mesopic foveal contrast sensitivity is impaired in diabetic patient without retinopathy. Graef Arch Clin Exp Ophthalmol. 2010;248(12):1699-1703.
  45. Nordmann JP, Saraux H, Roullet E. Contrast sensitivity in Multiple sclerosis in 35 patients with and without optic neuritis. Ophtalmologica 1987;195(4):199-204.
  46. de Marco R, Ambrosio G, Ferrara G. Measuring contrast sensitivity in patients with Gravese ophthalmolopathy complicated by ocular hypertension and suspect glaucoma or dysthyroid optic neuropathy. Doc Ophthalmol. 2000;101(4):165-177.
  47. Fledelius HC, Fuchs J, Reck A. Refraction in diabetics during metabolic dysregulation, acute and chronic. With special reference to the diabetic myopia concept. Acta Ophthalmol. 1990;68(3):275-280.
  48. Oklamoto F, Sone H, Nonoyama T, Hommura S. Refractive chages in diabetic patients during intensive glycaemic control. Br J Ophthalmol. 2000;84(10):1097-1102.
  49. Kato S, Shiokawa A, Fukushima H, et al. Glycemic control and lens transparency in patients with type 1 diabetes mellitus. Am J Ophthalmol. 2001;131(3):301-304.
  50. Malone JI, Lowitt S, Cook WR. Nonosmotic diabetic cataracts. Pediatr Res. 1990;27(6):293-296.
  51. Krásný J, Vyplašilová E, Brunnerová R, et al. Změna transparence čočky u dětí, mladistvých a mladých dospělých s diabetes mellitus 1. typu [The human lens´transparence changes in children, adolescent, and young aduls]. Cesk Slov Oftal. 2006;62(5):304-314. Czech.
  52. Cornwell M, Lepre F. Acute irreversible cataracts in diabetes mellitus. Aust N Z J Ophthalmol. 1999;23(3):221-222.
  53. Orts VP, Devesa TP, Belmonte MJ. Juvenile diabetic cataract. A rare finding which lead us to diagnosis of this illness. Arch Soc Esp Ofalmnol. 2003;78(7):389-391. Spanish.
  54. Ewing FM, Deary IJ, Strachan MW, Frier BM. Seeing beyond retinopathy in diabetes: electrophysiological and psychophysical abnormalities and alterations in vision. Endocr Res. 1998;19(4):462-476.
  55. Ong GL, Ripley LG, Newsom RS, Casswell AG. Assessment of color vision as a screening test for sight threatening diabetic retinopathy before loss of vision. Br J Ophthalmol. 2003;87(6):747-752.
  56. Barton FB, Fong DS, Knatterund GL; ETDRS Research Group. Clůassification of Farnworth-Munsell 100 hue-test results in the early treatment diabetic retinopathy study. Am J Ophthalmol. 2004;138(1):119-124.
  57. Mortlock KE, Chiti Z, Drasdo N, Owens DR, North RV. Silent substitution A-cone elektroretinogram in subjects with diabetes mellitus. Ophthalmic Physiol Opt. 2005;25(5):322-329.
  58. Holm K, Larsson J, Lövestam-Adrian M. In diabetic retinopathy, foveolal thickness of 3900 mum seems to correlate with functionally significant loss of vision. Doc Ophthalmol. 2007;114(3):117-124.
  59. Sacconi R, Casaluci M, Borrelli E, et al. Multimodal paging assessment of vascular and neurodegenerative retinal alterations in type 1 diabetic patiens without fundoscopic sings of diabetic retinopapthy. J Clin Med. 2019 Sep 8;8(9):1409. doi: 10.3390/jcm8091409.
  60. Sacconi R, Lamanna F, Borrelli E, et al. Morphofunctional analysis of the retina in patients with type 1 diabetes without complicatins after 309 years of disease. Sci Rep. 2020 Jan 14;10(1):206. doi: 10.1038/s41598-019-57034-1.
  61. Koleva-Georgieva DN, Sivkova NP. Optical coherence tomography for the detection of early macular edema in diabetic patients with retinopathy. Folia Med (Plovdiv) 2010;52(1):40-48.
  62. Sanchez-Tocino H. Alvarez-Vidal A, Maldonado MS, Morena-montanes J, Gorcha-Layana A. Retinal thickness study with optical coherence tomography in patients with diabetes. Invest Ophthalmol Vis Sci. 2002;43(5):1588-1794.
  63. Sabouri MR, Kazemnezhad E, Hafezi V. Assessment of macular thickness in healthy eyes using Cirrus HD-OCT: a cross-sectional study. Med Hypothesis Discov Innov Ophthalmol. 2016;5(3):104-111.
  64. Vujosevic S, Bini S, Midena G, Berton M, Pilotto E, Midena E. Hyperreflectoive intraretinal spots in diabetics without and with nonproliferative diabetic retinopathy: an in vivo study using Spectral Domain OCT. J Diabetes Res 2013; 2013 Dec 9. doi: 10.1155/2013/491835
  65. Framme C, Schweizer P, Imesch M, Wolf S, Wolf-Schnurrbusch U. Behaviuor of SD-OCT detected hypperreflective foci in the retina of anti-VEGF treated patients with macular edema. Invest Ophthalmol Vis Sci. 2012;53(9):5814-5818.
  66. Enders C, Baeuerle F, Lang GE, et al. Comparison between findings in optical coherence tomography angiogramy in fluorescein angiogramy in patiens with diabetic retinopathy. Ophthalmologica 2019;28(1):1-6.
  67. Mihailovic N, Eter N, Alnawaiseh M. Foveolar avasculare zone OCT angiogramy. An overview of current knowledge. Ophthalmologe. 2019;116(7):610-616.
  68. Ashraf M, Nesper PL,Jampo LM, Yu F, Fawzi AA. Statistical model of optical coherence Tomography angiogramy parameters that correlate with severity of diabetic retinopathy. Invest Ophtalmol Vis Sci. 2018;59(10):4292-4298.
  69. Ishii H, Shoji T, Yoshikawa Y, Kanno J, Ibuki H, Shinoda K. Automated measurement of the foveal avascular zone in swept-source optical coherence tomography angiography images. Transl Vis Sci Technol. 2019;8(3):28. doi:10.1167/tvst.8.3.28.
  70. Munk MR, Giannakaki-Zimmermann H, Berger L, et al. OCT-angiography. A qualitative and quantitative comparison of 4 OCT-A devices. PLoS One. 2017 May 10; 12(5):e0177059.
  71. Ruminski D, Sikorski BL, Bukowska D, et al. OCT angiogramy by absolute intensity diference applied to norma l diseased human retinas. Biomedcal Optics Express. 2015;6(8):2738-2754.
  72. Bates NM, Tian J, Smiddy WE, et al. Relationship between the morfology of the foveal avascular zone, retinal structure, and macular circulation in patiens with diabetes mellitus. Sci Rep. 2018;8(1):5355. doi:10.1038/sr41598-018-23604-y
  73. Miwa Y, Murakami T, Suzuma K, et al. Relationship between functional and structural changes in diabetic vessels in optical coherence tomography angiography. Scintific Reports. 2016;6: e29064.
  74. Parravano M, De Geronimo D, Scarinci F, et al. Relationship between internal reflectivity of diabetic microaneurysms on SD.OCT and detection on OCT angiography. Am J Ophthalmol. 2017 May 5; doi: 10.1016/j.ajo.2017,04.021
  75. Ishibazawa A, Nagaoka T, Takahashi A, et al. Optical coherence tomography angiography in diabetic retinopathy: a prospective study. Am J Ophthalmol. 2015;160(1):35-44.
  76. Xu X, Chen C, Ding W, et al. Automated quantification of superficial retinal capillaries and large vessels for diabetic retinopathy on optical coherence tomography angiography. J Biophotonics. 2019 Nov; 12(11): e201900103.
  77. de Carlo TE, Chin RT, Bonini MA, et al. Detection of microvascular changes in eyes of patients with diabetes but not clinical diabetic retinopathy using optical coherence tomography angiography. Retina 2015;35(11):2364-2370.
  78. Gildea D. The diagnostic value of optical coherence tomography angiography in diabetic retinopathy: a systematic review. Int Ophthalmol. 2019;39(10):2413-2433.
  79. Inanc M, Tekin K, Kizitoprak 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 Opthalmol. 2019;207(1):37-44.
  80. Simonett JM, Scarinci F, Piccconi F, et al. Early microcircular retinal changes in optical coherence tomography angiography in patients with type 1 diabetes mellitus. Acta ophthalmol 2019;257(4):689-697.
  81. Sousa DC, Leal I, Moreire S, et al. Optical coherence tomography angiography study of the retinal vascular plexus in type 1 diabetes without retinopathy. Eye (London) 2019;34(2)307-311.
  82. Sambhav K, Abu-Almero KK, Chalam KV. Deep capillary macular perfusion indices obtained with OCT angiography correlate with degree of nonproliferative diabetic retinopathy. Eur J ophthamol. 2017 Mar 27; doi:5301/ejo.5000948
  83. Rosen RB, Andrade Romo JS, Krawitz BD, et al. Earliest evidence of preclinical diabetic retinopathy revealed using optical coherence tomography angiography perfused capillary density. Am J Ophthalmol. 2019 Jul;203:103. doi:10.1016/j ajo.2019.01.012
  84. Sun Z, Tang F, Wing R, et al. OCT angiography metrics predict progression of diabetic retinopathy and development of diabetic macular edema: a prospective study. Ophthalmology 2019; 126(12):1675-1684.
  85. Sousa DC, Leal I, Moreira S, et al. Optical coherence tomography angiography study of the retinal vascular plexus in type 1 diabetes without retinopathy. Eye (London) 2020 Feb;34(2):307-311.
  86. Botto de Barros Garcia JM, Leonardo D. Diabetic retinopathy and OCT angiography: clinical findings and future perspectives. Int J Retina Vitreous 2017 Mar 13;3. doi:1186/s400942-017-0062-2
  87. Bontzos G, Kabanarou SA, Gkizis I, Ragkousis A, Xirou T, Peto T. Retinal neurodegeneration, macular circulation and morfology of the foveal avascular zone in diabetic patiens: quantitative cross-sectional study usung OCT-A. Acta Ophthalmol. 2021 Jan 10; doi:10.1111/aos.14754
  88. Endo H, Kase S, Takahashi M, et al. Alteration of layer thickness in the choroid of diabetic patients. Clin Exp Ophthalmol. 2018 May 9; doi:10.1111/ceo.13299
  89. Tavares-Ferreira J, Vincente A, Proenca R. Choroidal thickness in diabetic patients without diabetic retinopathy. Retina. 2018;38(4):795-804.
  90. Orduna-Hospital E, Perdices L, Sanchez-Cano A, Acha J, Cueca N, Pinilla I. Choroidal changes of long-term type 1 diabetic patients without retinopathy. Diagnostics (Basel) 2020 Apr 19; 10(4). doi:10.3390/diagnostics10040235
  91. Yülek F, Ugürlu N, Önal ED, et al. Choroidal changes and duration of diabetes. Semin Ophthalmol. 2014;29(2):80-84.
  92. Sala-Puigdollers A, Figueras-Roco M, Hereu M, et al. Repeatability and reproductibility of retinal and choriodal thickness measurements in diabetic macular edema using swept-source optical coherence tomography. PLos One. 2018 Jul;13(7). e200819.
  93. Torabi H, Isfeedvajani MS, Ramezani M, Daryabari SH. Choroidal thickness and Haemoglobin A1c levels in patients with Type 2 diabetes mellitus. J Ophthamol Vis Res. 2019;14(3):285-290.
  94. Klein R, Klein BE, Moss SE, Cruickshanks KJ. The Wisconsin epidemiologic study of diabetic retinopathy: XVII. The 14-years incidence and progression of diabetic retinopathy and associated risk factors in type 1 diabetes. Ophtalmology 1988;105(10):1801-1815.
  95. Klein R, Klein BE, Moss SE, at al. Retinal vascular abnormalities in persons with type 1 diabetes. Ophthalmology. 2003;110(12):2118-2125.
  96. Klein R, Lee KE, Gangnon RE, Klein BE. The 25-year incidence of visual impairment in type 1 diabetes mellitus: the Wisconsin epidemiologic study of diabetic retinopathy. Ophthalmology. 2010;117(1):63-70.
  97. Evertsen J, Alemzadeh R, Wang X. Increasing incidence of pediatric type 1 diabetes mellitus in Southeastern Wisconsin: relationship with body weight at diagnosis. PLos One. 2009 Sep 3;4(9): e6873.
  98. Kilpatrick ES, Rigby AS, Atkin SL. HbA1C variability and the risk of microvascular complication in type 1 diabetes: data from Diabetes Control and Complication Trial. Diabetes Care. 2008;31(11):2198-2202.
  99. Waden J, Forsblom C; Finish Diabetic Nephropathy Study Group. Hb1AC variability predict incident cardiovascular events, microalubinuria, and overt diabetic nephropathy in patients with type 1diabetes. Diabetes. 2009; 58(11):2649-2655.
  100. Moon SW, Kim HY, Kim SW, Oh J, Huh K, Oh IK. The change of macular thickness measured by optical coherence tomography in relation to glycemic control in diabetic patients. Graef Arch Clin Exp Ophthalmol. 2011;249(6):639-648.
  101. Kilpatrick ES, Rigby AS, Atkin SL. Effect of glucose variability on the long-term risk of microvascular complication in type 1 diabetes. Diabetes Care. 2006;29(7):1486-1490.
  102. Diabetes Control and Complication Trial Research Group / Epidemiology of Diabetes Interventions and Complications Study Research Group. Long-term effect of diabetes and its treatment on cognitive function. N Eng J Med. 2007;356(18):1542-1452.
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