Ophthalmic Research

Research Article

The Effect of Glycemia on Choroidal Thickness in Different Stages of Diabetic Retinopathy

Abalem M.F.a,b · Nazareth Santos Veloso H.a · Garcia R.a · Chen X.D.b · Carricondo P.C.a · Cabral Zacharias L.a · Preti R.C.a

Author affiliations

aDivision of Ophthalmology, University of São Paulo Medical School, São Paulo, Brazil
bDepartment of Ophthalmology and Visual Sciences, Kellogg Eye Center, University of Michigan, Ann Arbor, MI, USA

Keywords: DiabetesDiabetic retinopathyOptical coherence tomographyRetinaChoroidGlucose

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Ophthalmic Res 2020;63:474–482
https://doi.org/10.1159/000506381

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Article / Publication Details

First-Page Preview
Abstract of Research Article

Received: November 08, 2019
Accepted: February 02, 2020
Published online: February 10, 2020
Issue release date: August 2020

Number of Print Pages: 9
Number of Figures: 2
Number of Tables: 3

ISSN: 0030-3747 (Print)
eISSN: 1423-0259 (Online)

For additional information: https://www.karger.com/ORE

Abstract

Objective: The purpose of this study was to evaluate the influence of renal and glycemic parameters on choroidal thickness (CT) in patients with diabetes with and without diabetic retinopathy (DR). Methods: This cross-sectional study included patients with and without diabetes. Patients underwent comprehensive ocular examination. CT was obtained using spectral-domain optical coherence tomography (SD-OCT) with enhanced depth imaging (EDI) mode. Clinical parameters were body mass index, mean arterial pressure, glycated hemoglobin, fasting plasma glucose, estimated glomerular filtration rate, and capillary plasma glucose (CPG) a few minutes before EDI-SD-OCT. Results: The study included 275 participants: 42 with diabetes and no DR, 43 with mild nonproliferative diabetic retinopathy (NPDR), 46 with moderate NPDR, 39 with severe NPDR, 24 with proliferative diabetic retinopathy (PDR), 40 with previous panretinal photocoagulation (PRP) treatment for DR, and 41 without diabetes. The diabetic patients had thinner subfoveal CT than the nondiabetic participants (280.5 ± 83.4 vs. 327.1 ± 48.8 µm, p < 0.001). After multivariable adjustment, CT was significantly correlated with age, DR stage, and CPG. In patients with mild and moderate NPDR, a higher level of CPG was associated with thicker CT. This relationship was not found in patients with PDR. Conclusion: CPG had the strongest correlation with CT in patients with NPDR (mild, moderate, and severe), but not in PDR and PRP PDR patients. Our study suggests that the glucose level at the time of the test should be aggregated to other systemic and ocular parameters, such as age and axial length, when studying the choroid using SD-OCT.

© 2020 S. Karger AG, Basel



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References

  1. Lutty GA. Effects of diabetes on the eye. Invest Ophthalmol Vis Sci. 2013 Dec;54(14):ORSF81-7.
    External Resources
  2. Laíns I, Figueira J, Santos AR, Baltar A, Costa M, Nunes S, et al. Choroidal thickness in diabetic retinopathy: the influence of antiangiogenic therapy. Retina. 2014 Jun;34(6):1199–207.
    External Resources
  3. Tan CS, Ouyang Y, Ruiz H, Sadda SR. Diurnal variation of choroidal thickness in normal, healthy subjects measured by spectral domain optical coherence tomography. Invest Ophthalmol Vis Sci. 2012 Jan;53(1):261–6.
    External Resources
  4. Iwase T, Yamamoto K, Kobayashi M, Ra E, Murotani K, Terasaki H. What ocular and systemic variables affect choroidal circulation in healthy eyes. Medicine (Baltimore). 2016 Oct;95(43):e5102.
    External Resources
  5. Goldenberg D, Moisseiev E, Goldstein M, Loewenstein A, Barak A. Enhanced depth imaging optical coherence tomography: choroidal thickness and correlations with age, refractive error, and axial length. Ophthalmic Surg Lasers Imaging. 2012 Jul;43(4):296–301.
    External Resources
  6. Germano RA, Hatanaka M, Susanna R. Choroidal thickness variation in highly myopic eyes during the water drinking test. Arq Bras Oftalmol. 2016 Jul–Aug;79(4):214–7.
    External Resources
  7. Mansouri K, Medeiros FA, Marchase N, Tatham AJ, Auerbach D, Weinreb RN. Assessment of choroidal thickness and volume during the water drinking test by swept-source optical coherence tomography. Ophthalmology. 2013 Dec;120(12):2508–16.
    External Resources
  8. Yiu G, Manjunath V, Chiu SJ, Farsiu S, Mahmoud TH. Effect of anti-vascular endothelial growth factor therapy on choroidal thickness in diabetic macular edema. Am J Ophthalmol. 2014 Oct;158(4):745–751.e2.
    External Resources
  9. Esen E, Sizmaz S, Demircan N. Choroidal thickness changes after intravitreal dexamethasone implant injection for the treatment of macular edema due to retinal vein occlusion. Retina. 2016 Dec;36(12):2297–303.
    External Resources
  10. Zhang Z, Meng X, Wu Z, Zou W, Zhang J, Zhu D, et al. Changes in Choroidal Thickness After Panretinal Photocoagulation for Diabetic Retinopathy: A 12-Week Longitudinal Study. Invest Ophthalmol Vis Sci. 2015 Apr;56(4):2631–8.
    External Resources
  11. Zengin MO, Cinar E, Kucukerdonmez C. The effect of nicotine on choroidal thickness. Br J Ophthalmol. 2014 Feb;98(2):233–7.
    External Resources
  12. Vural AD, Kara N, Sayin N, Pirhan D, Ersan HB. Choroidal thickness changes after a single administration of coffee in healthy subjects. Retina. 2014 Jun;34(6):1223–8.
    External Resources
  13. Ferreira CS, Beato J, Falcao MS, Brandao E, Falcao-Reis F, Carneiro AM. Choroidal thickness in multisystemic autoimmune diseases without ophthalmologic manifestations. Retina. 2017 Mar;37(3):529–35.
  14. Abalem MF, Machado MC, Santos HN, Garcia R, Helal J Jr, Carricondo PC, et al. Choroidal and Retinal Abnormalities by Optical Coherence Tomography in Endogenous Cushing’s Syndrome. Front Endocrinol (Lausanne). 2016 Dec;7:154.
    External Resources
  15. Akay F, Gundogan FC, Yolcu U, Toyran S, Uzun S. Choroidal thickness in systemic arterial hypertension. Eur J Ophthalmol. 2016 Mar–Apr;26(2):152–7.
    External Resources
  16. 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):423–8.
    External Resources
  17. Balmforth C, van Bragt JJ, Ruijs T, Cameron JR, Kimmitt R, Moorhouse R, et al. Chorioretinal thinning in chronic kidney disease links to inflammation and endothelial dysfunction. JCI Insight. 2016 Dec;1(20):e89173.
    External Resources
  18. Chang IB, Lee JH, Kim JS. Changes in choroidal thickness in and outside the macula after hemodialysis in patients with end-stage renal disease. Retina. 2017 May;37(5):896–905.
  19. Ishibazawa A, Nagaoka T, Minami Y, Kitahara M, Yamashita T, Yoshida A. Choroidal Thickness Evaluation Before and After Hemodialysis in Patients With and Without Diabetes. Invest Ophthalmol Vis Sci. 2015 Oct;56(11):6534–41.
    External Resources
  20. Klefter ON, Vilsbøll T, Knop FK, Larsen M. Retinal vascular and structural dynamics during acute hyperglycaemia. Acta Ophthalmol. 2015 Dec;93(8):697–705.
    External Resources
  21. Melancia D, Vicente A, Cunha JP, Abegão Pinto L, Ferreira J. Diabetic choroidopathy: a review of the current literature. Graefes Arch Clin Exp Ophthalmol. 2016 Aug;254(8):1453–61.
    External Resources
  22. Aiello LP, Gardner TW, King GL, Blankenship G, Cavallerano JD, Ferris FL 3rd, et al. Diabetic retinopathy. Diabetes Care. 1998 Jan;21(1):143–56.
    External Resources
  23. Antonetti DA, Klein R, Gardner TW. Diabetic retinopathy. N Engl J Med. 2012 Mar;366(13):1227–39.
    External Resources
  24. Jawa A, Kcomt J, Fonseca VA. Diabetic nephropathy and retinopathy. Med Clin North Am. 2004 Jul;88(4):1001–36, xi.
    External Resources
  25. Khalil H. Diabetes microvascular complications – a clinical update. Diabetes Metab Syndr. 2017 Nov;11(Suppl 1):S133–9.
    External Resources
  26. Lutty GA. Diabetic choroidopathy. Vision Res. 2017 Oct;139:161–7.
    External Resources
  27. Saker S, Stewart EA, Browning AC, Allen CL, Amoaku WM. The effect of hyperglycaemia on permeability and the expression of junctional complex molecules in human retinal and choroidal endothelial cells. Exp Eye Res. 2014 Apr;121:161–7.
    External Resources
  28. American Diabetes Association. Standards of medical care in diabetes – 2014. Diabetes Care. 2014 Jan;37(Suppl 1):S14–80.
    External Resources
  29. Photocoagulation for diabetic macular edema. Early Treatment Diabetic Retinopathy Study report number 1. Early Treatment Diabetic Retinopathy Study research group. Arch Ophthalmol. 1985 Dec;103(12):1796–806.
  30. Little RR, Rohlfing CL, Wiedmeyer HM, Myers GL, Sacks DB, Goldstein DE; NGSP Steering Committee. The national glycohemoglobin standardization program: a five-year progress report. Clin Chem. 2001 Nov;47(11):1985–92.
    External Resources
  31. Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D; Modification of Diet in Renal Disease Study Group. A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Ann Intern Med. 1999 Mar;130(6):461–70.
    External Resources
  32. Nickla DL, Wallman J. The multifunctional choroid. Prog Retin Eye Res. 2010 Mar;29(2):144–68.
    External Resources
  33. Blaauwgeers HG, Holtkamp GM, Rutten H, Witmer AN, Koolwijk P, Partanen TA, et al. Polarized vascular endothelial growth factor secretion by human retinal pigment epithelium and localization of vascular endothelial growth factor receptors on the inner choriocapillaris. Evidence for a trophic paracrine relation. Am J Pathol. 1999 Aug;155(2):421–8.
    External Resources
  34. Cao J, McLeod S, Merges CA, Lutty GA. Choriocapillaris degeneration and related pathologic changes in human diabetic eyes. Arch Ophthalmol. 1998 May;116(5):589–97.
    External Resources
  35. Shiba C, Shiba T, Takahashi M, Matsumoto T, Hori Y. Relationship between glycosylated hemoglobin A1c and ocular circulation by laser speckle flowgraphy in patients with/without diabetes mellitus. Graefes Arch Clin Exp Ophthalmol. 2016 Sep;254(9):1801–9.
    External Resources
  36. Yazgan S, Arpaci D, Celik HU, Dogan M, Isık I. Macular choroidal thickness may be the earliest determiner to detect the onset of diabetic retinopathy in patients with prediabetes: a prospective and comparative study. Curr Eye Res. 2017 Jul;42(7):1039–47.
    External Resources
  37. 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 Ophthalmol Vis Sci. 2013 May;54(5):3378–84.
    External Resources
  38. Lee SH, Kim J, Chung H, Kim HC. Changes of choroidal thickness after treatment for diabetic retinopathy. Curr Eye Res. 2014 Jul;39(7):736–44.
    External Resources
  39. Querques G, Lattanzio R, Querques L, Del Turco C, Forte R, Pierro L, et al. Enhanced depth imaging optical coherence tomography in type 2 diabetes. Invest Ophthalmol Vis Sci. 2012 Sep;53(10):6017–24.
    External Resources
  40. Esmaeelpour M, Považay B, Hermann B, Hofer B, Kajic V, Hale SL, et al. Mapping choroidal and retinal thickness variation in type 2 diabetes using three-dimensional 1060-nm optical coherence tomography. Invest Ophthalmol Vis Sci. 2011 Jul;52(8):5311–6.
    External Resources
  41. Kase S, Endo H, Yokoi M, Kotani M, Katsuta S, Takahashi M, et al. Choroidal thickness in diabetic retinopathy in relation to long-term systemic treatments for diabetes mellitus. Eur J Ophthalmol. 2016 Mar–Apr;26(2):158–62.
    External Resources
  42. Çalişkan S, Uğurbaş SC, Alpay A, Uğurbaş SH. Changes in the Choroidal Thickness and Axial Length Upon Mannitol Infusion in Patients With Asymmetric Intraocular Pressure. J Glaucoma. 2016 Nov;25(11):891–5.
    External Resources
  43. Li Z, Zeng J, Jin W, Long W, Lan W, Yang X. Time-Course of Changes in Choroidal Thickness after Complete Mydriasis Induced by Compound Tropicamide in Children. PLoS One. 2016 Sep;11(9):e0162468.
    External Resources
  44. Wallman J, Wildsoet C, Xu A, Gottlieb MD, Nickla DL, Marran L, et al. Moving the retina: choroidal modulation of refractive state. Vision Res. 1995 Jan;35(1):37–50.
    External Resources
  45. Rada JA, Palmer L. Choroidal regulation of scleral glycosaminoglycan synthesis during recovery from induced myopia. Invest Ophthalmol Vis Sci. 2007 Jul;48(7):2957–66.
    External Resources
  46. Pendrak K, Papastergiou GI, Lin T, Laties AM, Stone RA. Choroidal vascular permeability in visually regulated eye growth. Exp Eye Res. 2000 May;70(5):629–37.
    External Resources
  47. Rymer J, Wildsoet CF. The role of the retinal pigment epithelium in eye growth regulation and myopia: a review. Vis Neurosci. 2005 May–Jun;22(3):251–61.
    External Resources
  48. Stübinger K, Brehmer A, Neuhuber WL, Reitsamer H, Nickla D, Schrödl F. Intrinsic choroidal neurons in the chicken eye: chemical coding and synaptic input. Histochem Cell Biol. 2010 Aug;134(2):145–57.
    External Resources

Article / Publication Details

First-Page Preview
Abstract of Research Article

Received: November 08, 2019
Accepted: February 02, 2020
Published online: February 10, 2020
Issue release date: August 2020

Number of Print Pages: 9
Number of Figures: 2
Number of Tables: 3

ISSN: 0030-3747 (Print)
eISSN: 1423-0259 (Online)

For additional information: https://www.karger.com/ORE

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