Macular Choroidal Thickness May Be the Earliest Determiner to Detect the Onset of Diabetic Retinopathy in Patients with Prediabetes: A Prospective and Comparative Study

References

• Lamparter J, Raum P, Pfeiffer N, Peto T, Höhn R, Elflein H, et al. Prevalence and associations of diabetic retinopathy in a large cohort of prediabetic subjects: the Gutenberg Health Study. J Diabetes Complications 2014 Jul–Aug;28(4):482–487.
   PubMed Web of Science ®Google Scholar
• American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2010 Jan;33 Suppl 1:S62–S69.
   PubMed Web of Science ®Google Scholar
• Tabák AG, Herder C, Rathmann W, Brunner EJ, Kivimäki M. Prediabetes: a high-risk state for diabetes development. Lancet 2012 Jun 16;379(9833):2279–2290.
   PubMed Web of Science ®Google Scholar
• Salazar MR, Carbajal HA, Espeche WG, Aizpurúa M, Leiva Sisnieguez CE, Leiva Sisnieguez BC, et al. Insulin resistance: the linchpin between prediabetes and cardiovascular disease. Diab Vasc Dis Res 2016 Mar;13(2):157–163.
   PubMed Web of Science ®Google Scholar
• Giráldez-García C, Sangrós FJ, Díaz-Redondo A, Franch-Nadal J, Serrano R, Díez J, et al. Cardiometabolic risk profiles in patients with impaired fasting glucose and/or hemoglobin A1c 5.7% to 6.4%: evidence for a gradient according to diagnostic criteria: the PREDAPS Study. Medicine (Baltimore) 2015 Nov;94(44):e1935.
   PubMed Web of Science ®Google Scholar
• Nickla DL, Wallman J. The multifunctional choroid. Prog Retin Eye Res 2010 Mar;29(2):144–168.
   PubMed Web of Science ®Google Scholar
• Kim JT, Lee DH, Joe SG, Kim JG, Yoon YH. Changes in choroidal thickness in relation to the severity of retinopathy and macular edema in type 2 diabetic patients. Invest Ophtalmol Vis Sci 2013 May 9;54(5):3378–3384.
   PubMed Web of Science ®Google Scholar
• Kanski JJ, Bowling B. Retinal Vascular Diseases. Clinical Ophthalmology: A Systematic Approach. Elsevier, UK (Volume 13, 7th edition, p. 534), 2011.
   Google Scholar
• Milman S, Crandall JP. Mechanisms of vascular complications in prediabetes. Med Clin North Am 2011 Mar;95(2):309–325.
   PubMed Web of Science ®Google Scholar
• Gabir MM, Hanson RL, Dabelea D, Imperatore G, Roumain J, Bennett PH, et al. Plasma glucose and prediction of microvascular disease and mortality: evaluation of 1997 American Diabetes Association and 1999 World Health Organization criteria for diagnosis of diabetes. Diabetes Care 2000 Aug;23(8):1113–1118.
   PubMed Web of Science ®Google Scholar
• Algvere P, Efendić S, Luft R, Wajngot A. Retinal microangiopathy and pigment epithelial lesions in subjects with normal, borderline, and decreased oral glucose tolerance. Br J Ophthalmol 1985 Jun;69(6):416–419.
   PubMed Web of Science ®Google Scholar
• Tapp RJ, Tikellis G, Wong TY, Harper CA, Zimmet PZ, Shaw JE. Longitudinal association of glucose metabolism with retinopathy: results from the Australian Diabetes Obesity and Lifestyle (AusDiab) study. Diabetes Care 2008;31:1349–1354.
   PubMed Web of Science ®Google Scholar
• Nguyen TT, Wang JJ, Wong TY. Retinal vascular changes in pre-diabetes and prehypertension: new findings and their research and clinical implications. Diabetes Care 2007;30(10):2708–2715.
   PubMed Web of Science ®Google Scholar
• Lott ME, Slocomb JE, Shivkumar V, Smith B, Quillen D, Gabbay RA, et al. Impaired retinal vasodilator responses in prediabetes and type 2 diabetes. Acta Ophthalmol 2013 Sep;91(6):e462–e469.
   PubMed Web of Science ®Google Scholar
• Spaide RF, Koizumi H, Pozonni MC. Enhanced depth imaging spectral-domain optical coherence tomography. Am J Ophthalmol 2008;46:496–500.
   Web of Science ®Google Scholar
• Mehlsen J, Wiinberg N. Interarm difference in blood pressure: reproducibility and association with peripheral vascular disease. Int J Vasc Med 2014;2014:841542.
   PubMedGoogle Scholar
• Kohner E, Porta M. Vascular abnormalities in diabetes and their treatment. Trans Ophthalmol Soc UK 1980;100:400–444.
   PubMedGoogle Scholar
• Joussen AM, Poulaki V, Le ML, Koizumi K, Esser C, Janicki H, et al. A central role for inflammation in the pathogenesis of diabetic retinopathy. FASEB J 2004 Sep;18(12):1450–1452.
   PubMed Web of Science ®Google Scholar
• Klein R, Klein BE, Moss SE, Davis MD, De Mets DL. Glycosylated hemoglobin predicts the incidence and progression of diabetic retinopathy. JAMA 1988 Nov 18;260(19):2864–2871.
   PubMed Web of Science ®Google Scholar
• The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N Engl J Med 1993 Sep 30;329(14):977–986.
   PubMed Web of Science ®Google Scholar
• Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) Group. Lancet 1998 Sep 12;352(9131):837–853.
   PubMed Web of Science ®Google Scholar
• Tight blood pressure control and risk of macrovascular and microvascular complications in type 2 diabetes: UKPDS 38. UK Prospective Diabetes Study Group. BMJ 1998 Sep 12;317(7160):703–713.
   Google Scholar
• Wong TY, Barr EL, Tapp RJ, Harper CA, Taylor HR, Zimmet PZ, et al. Retinopathy in persons with impaired glucose metabolism: the Australian Diabetes Obesity and Lifestyle (AusDiab) study. Am J Ophthalmol 2005 Dec;140(6):1157–1159.
   PubMed Web of Science ®Google Scholar
• Diabetes Prevention Program Research Group. The prevalence of retinopathy in impaired glucose tolerance and recent-onset diabetes in the Diabetes Prevention Program. Diabet Med 2007 Feb;24(2):137–144.
   PubMed Web of Science ®Google Scholar
• Kanski JJ, Bowling B. Retinal Vascular Diseases. Clinical Ophthalmology: A Systematic Approach. Elsevier, UK (Volume 13, 7th edition, p. 535), 2011.
   Google Scholar
• Ikram MK, Janssen JA, Roos AM, Rietveld I, Witteman JC, Breteler MM, et al. Retinal vessel diameters and risk of impaired fasting glucose or diabetes: the Rotterdam study. Diabetes 2006 Feb;55(2):506–510.
   PubMed Web of Science ®Google Scholar
• Cao J, McLeod S, Merges CA, Lutty GA. Choriocapillaris degeneration and related pathologic changes in human diabetic eyes. Arch Ophthalmol 1998 May;116(5):589–597.
   PubMedGoogle Scholar
• Fukushima I, McLeod DS, Lutty GA. Intrachoroidal microvascular abnormality: a previously unrecognized form of choroidal neovascularization. Am J Ophthalmol 1997;124:473–487.
   PubMed Web of Science ®Google Scholar
• Hidayat AA, Fine BS. Diabetic choroidopathy. Light and electron microscopic observations of seven cases. Ophthalmology 1985;92(4):512–522.
   Google Scholar
• McLeod DS, Lutty GA. High-resolution histologic analysis of the human choroidal vasculature. Invest Ophthalmol Vis Sci 1994 Oct;35(11):3799–3811.
   PubMed Web of Science ®Google Scholar
• Lutty GA, Cao J, McLeod DS. Relationship of polymorphonuclear leukocytes to capillary dropout in the human diabetic choroid. Am J Pathol 1997;151(3):707–714.
   PubMed Web of Science ®Google Scholar
• Lee SH, Kim J, Chung H, Kim HC. Changes of choroidal thickness after treatment for diabetic retinopathy. Curr Eye Res 2014 Jul;39(7):736–744.
   PubMed Web of Science ®Google Scholar
• van Leiden HA, Dekker JM, Moll AC, Nijpels G, Heine RJ, Bouter LM, Stehouwer CD, Polak BC. Blood pressure, lipids, and obesity are associated with retinopathy: the Hoorn study. Diabetes Care 2002 Aug;25(8):1320–1325.
   PubMed Web of Science ®Google Scholar
• Wong IY, Wong RL, Zhao P, Lai WW. Choroidal thickness in relation to hypercholesterolemia on enhanced depth imaging optical coherence tomography. Retina 2013 Feb;33(2):423–428.
   PubMed Web of Science ®Google Scholar
• Yilmaz I, Ozkaya A, Kocamaz M, Ahmet S, Ozkaya HM, Yasa D, et al. Correlation of choroidal thickness and body mass index. Retina 2015 Oct;35(10):2085–2090.
   PubMed Web of Science ®Google Scholar
• Okamoto M, Matsuura T, Ogata N. Effects of panretinal photocoagulation on choroidal thickness and choroidal blood flow in patients with severe nonproliferative diabetic retinopathy. Retina 2016 Apr;36(4):805–811.
   PubMed Web of Science ®Google Scholar
• Sudhalkar A, Chhablani JK, Venkata A, Raman R, Rao PS, Jonnadula GB. Choroidal thickness in diabetic patients of Indian ethnicity. Indian J Ophthalmol 2015 Dec;63(12):912–916.
   PubMed Web of Science ®Google Scholar
• Esmaeelpour M, Brunner S, Ansari-Shahrezaei S, Nemetz S, Povazay B, Kajic V, Drexler W, Binder S. Choroidal thinning in diabetes type 1 detected by 3-dimensional 1060 nm optical coherence tomography. Invest Ophthalmol Vis Sci 2012 Oct 3;53(11):6803–6809.
   PubMed Web of Science ®Google Scholar
• Vujosevic S, Martini F, Cavarzeran F, Pilotto E, Midena E. Macular and peripapillary choroidal thickness in diabetic patients. Retina 2012;32(9):1781–1790.
   PubMed Web of Science ®Google Scholar
• Hu FB, Meigs JB, Li TY, Rifai N, Manson JE. Inflammatory markers and risk of developing type 2 diabetes in women. Diabetes 2004 Mar;53(3):693–700.
   PubMed Web of Science ®Google Scholar
• Sonoda S, Sakamoto T, Yamashita T, Otsuka H, Shirasawa M, Kakiuchi N, Uchino E, Terasaki H, Kawano H. Effect of intravitreal triamcinolone acetonide or bevacizumab on choroidal thickness in eyes with diabetic macular edema. Invest Ophthalmol Vis Sci 2014 Jun 6;55(6):3979–3985.
   PubMed Web of Science ®Google Scholar
• Karlica D, Galetović D, Ivanisević M, Skrabić V, Znaor L, Jurisić D. Visual evoked potential can be used to detect a prediabetic form of diabetic retinopathy in patients with diabetes mellitus type I. Coll Antropol 2010 Jun;34(2):525–529.
   PubMedGoogle Scholar
• Al Shafaee M, Shenoy R, Bialasiewicz AA, Ganguly SS, Bhargava K. Macular function in prediabetic and diabetic Omani adults: a microperimetric evaluation. Eur J Ophthalmol 2011 Nov–Dec;21(6):771–776.
   PubMed Web of Science ®Google Scholar
• Ikuno Y, Maruko I, Yasuno Y, Miura M, Sekiryu T, Nishida K, et al. Reproducibility of retinal and choroidal thickness measurements in enhanced depth imaging and high-penetration optical coherence tomography. Invest Ophthalmol Vis Sci 2011;52:5536–5540. [ PubMed: 21508114]
   Google Scholar
• Ruia S, Saxena S, Gemmy Cheung CM, Gilhotra JS, Lai TY. Spectral domain optical coherence tomography features and classification systems for diabetic macular edema: a review. Asia Pac J Ophthalmol (Phila) 2016;5(5):360–367.
   PubMed Web of Science ®Google Scholar