193
Views
0
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

The Association Between Lipid Profile and Subfoveal Choroidal Thickness in Chinese Patients with Proliferative Diabetic Retinopathy Secondary to Type 2 Diabetes

, , &
Pages 2477-2489 | Received 03 May 2023, Accepted 27 Jul 2023, Published online: 17 Aug 2023

References

  • Hidayat AA, Fine BS. Diabetic choroidopathy. Light and electron microscopic observations of seven cases. Ophthalmology. 1985;92(4):512–522. doi:10.1016/S0161-6420(85)34013-7
  • Gaudric A, Coscas G, Bird AC. Choroidal ischemia. Am J Ophthalmol. 1982;94(4):489–498. doi:10.1016/0002-9394(82)90242-2
  • Spaide RF, Koizumi H, Pozzoni MC. Enhanced depth imaging spectral-domain optical coherence tomography. Am J Ophthalmol. 2008;146(4):496–500. doi:10.1016/j.ajo.2008.05.032
  • Cheung N, Mitchell P, Wong TY. Diabetic retinopathy. Lancet. 2010;376(9735):124–136. doi:10.1016/S0140-6736(09)62124-3
  • Yau JW, Rogers SL, Kawasaki R, et al. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care. 2012;35(3):556–564.
  • Frank RN. Diabetic retinopathy. N Engl J Med. 2004;350(1):48–58. doi:10.1056/NEJMra021678
  • Milluzzo A, Maugeri A, Barchitta M, et al. Epigenetic mechanisms in type 2 diabetes retinopathy: a systematic review. Int J Mol Sci. 2021;22(19):10502. doi:10.3390/ijms221910502
  • Milluzzo A, Barchitta M, Maugeri A, et al. Do nutrients and nutraceuticals play a role in diabetic retinopathy? A Systematic review. Nutrients. 2022;14(20):4430. doi:10.3390/nu14204430
  • Milluzzo A, Barchitta M, Maugeri A, et al. Body mass index is related to short term retinal worsening in type 2 diabetes patients treated with anticancer drugs. Minerva Endocrinol. 2022. doi:10.23736/S2724-6507.22.03653-3
  • Yamanouchi M, Mori M, Hoshino J, et al. Retinopathy progression and the risk of end-stage kidney disease: results from a longitudinal Japanese cohort of 232 patients with type 2 diabetes and biopsy-proven diabetic kidney disease. BMJ Open Diabetes Res Care. 2019;7(1):e000726. doi:10.1136/bmjdrc-2019-000726
  • Mule G, Vadalà M, La Blasca T, et al. Association between early-stage chronic kidney disease and reduced choroidal thickness in essential hypertensive patients. Hypertens Res. 2019;42(7):990–1000. doi:10.1038/s41440-018-0195-1
  • Chung JO, Park S-Y, Cho DH, et al. Associations between serum apolipoproteins, urinary albumin excretion rate, estimated glomerular filtration rate, and diabetic retinopathy in individuals with type 2 diabetes. Medicine. 2019;98(20):e15703. doi:10.1097/MD.0000000000015703
  • Rodriguez-Poncelas A, Mundet-Tudurí X, Miravet-Jiménez S, et al. Chronic kidney disease and diabetic retinopathy in patients with type 2 diabetes. PLoS One. 2016;11(2):e0149448. doi:10.1371/journal.pone.0149448
  • Wang J, Xin X, Luo W, et al. Anemia and diabetic kidney disease had joint effect on diabetic retinopathy among patients with type 2 diabetes. Invest Ophthalmol Vis Sci. 2020;61(14):25. doi:10.1167/iovs.61.14.25
  • Rajalakshmi R, Shanthi Rani CS, Venkatesan U, et al. Correlation between markers of renal function and sight-threatening diabetic retinopathy in type 2 diabetes: a longitudinal study in an Indian clinic population. BMJ Open Diabetes Res Care. 2020;8(1):e001325. doi:10.1136/bmjdrc-2020-001325
  • Cho A, Park HC, Lee Y-K, et al. Progression of diabetic retinopathy and declining renal function in patients with type 2 diabetes. J Diabetes Res. 2020;2020:8784139. doi:10.1155/2020/8784139
  • Zhuang X, Cao D, Yang D, et al. Association of diabetic retinopathy and diabetic macular oedema with renal function in southern Chinese patients with type 2 diabetes mellitus: a single-centre observational study. BMJ Open. 2019;9(9):e031194. doi:10.1136/bmjopen-2019-031194
  • Huo Y, GUO Y, Wang H, et al. Change regularity of adult subfoveal choroidal thickness with age and its influencing factors. Chin J Exp Ophthalmol. 2021;39(1):29–33.
  • Shao L, Wang Y, Xu J, et al. Subfoveal choroidal thickness of Chinese aged over 50 years and patients with diabetes mellitus and glaucoma. Chin J Ophthalmol. 2014;50(6):414–420.
  • Wei WB, Xu L, Jonas JB, et al. Subfoveal choroidal thickness: the Beijing Eye Study. Ophthalmology. 2013;120(1):175–180. doi:10.1016/j.ophtha.2012.07.048
  • Moussa M, Sabry D, Soliman W. Macular choroidal thickness in normal Egyptians measured by swept source optical coherence tomography. BMC Ophthalmol. 2016;16:138. doi:10.1186/s12886-016-0314-1
  • Flores-Moreno I, Lugo F, Duker JS, et al. The relationship between axial length and choroidal thickness in eyes with high myopia. Am J Ophthalmol. 2013;155(2):314–319 e1. doi:10.1016/j.ajo.2012.07.015
  • Asikgarip N, Temel E, Kıvrak A, et al. Choroidal structural changes and choroidal vascularity index in patients with systemic hypertension. Eur J Ophthalmol. 2022;32(4):2427–2432. doi:10.1177/11206721211035615
  • Romero-Trevejo JL, Fernández-Romero L, Delgado J, et al. Choroidal thickness and granulocyte colony-stimulating factor in tears improve the prediction model for coronary artery disease. Cardiovasc Diabetol. 2022;21(1):103. doi:10.1186/s12933-022-01538-0
  • Fernandez-Espinosa G, Orduna-Hospital E, Boned-Murillo A, et al. Choroidal and retinal thicknesses in type 2 diabetes mellitus with moderate diabetic retinopathy measured by swept source OCT. Biomedicines. 2022;10(9):2314. doi:10.3390/biomedicines10092314
  • Gun RD, Gümüş T, Kardaş ASY, et al. Acute effect of hyperbaric oxygen therapy on macular and choroidal thickness in patients with type 2 diabetes and diabetic foot ulcers: optical coherence tomography based study. Photodiagnosis Photodyn Ther. 2022;39:102926. doi:10.1016/j.pdpdt.2022.102926
  • Wang W, Li L, Wang J, et al. Macular choroidal thickness and the risk of referable diabetic retinopathy in type 2 diabetes: a 2-year longitudinal study. Invest Ophthalmol Vis Sci. 2022;63(4):9. doi:10.1167/iovs.63.4.9
  • Durusoy GK, Gumus G, Onay M, et al. Early choroidal structure and choroidal vascularity index change after carotid stenting. Photodiagnosis Photodyn Ther. 2022;38:102748. doi:10.1016/j.pdpdt.2022.102748
  • Wan J, Kwapong WR, Tao. W, et al. Choroidal changes in carotid stenosis patients after stenting detected by swept-source optical coherence tomography angiography. Curr Neurovasc Res. 2022;19(1):100–107. doi:10.2174/1567202619666220406092532
  • Altinkaynak H, Kara N, Sayın N, et al. Subfoveal choroidal thickness in patients with chronic heart failure analyzed by spectral-domain optical coherence tomography. Curr Eye Res. 2014;39(11):1123–1128. doi:10.3109/02713683.2014.898310
  • Krajewski P, Turczyńska M, Gołębiewska J, et al. Optical coherence tomography angiography findings in patients with chronic thromboembolic pulmonary hypertension. Retina. 2022;42(12):2354–2360. doi:10.1097/IAE.0000000000003607
  • Wong IY, Wong RL, Zhao P, et al. Choroidal thickness in relation to hypercholesterolemia on enhanced depth imaging optical coherence tomography. Retina. 2013;33(2):423–428. doi:10.1097/IAE.0b013e3182753b5a
  • Marta WM, Andrzej O, Marta B-W, et al. Choroidal thickness in children with type 1 diabetes depending on the pubertal status and metabolic parameters analyzed by optical coherence tomography. Sci Rep. 2021;11(1):19677. doi:10.1038/s41598-021-97794-3
  • Aydin E, Kazanci L, Balikoglu Yilmaz M, et al. Analysis of central macular thickness and choroidal thickness changes in patients with cardiovascular risk factors. Eye. 2020;34(11):2068–2075. doi:10.1038/s41433-020-0775-6
  • Wang H, Ramshekar A, Kunz E, et al. 7-ketocholesterol induces endothelial-mesenchymal transition and promotes fibrosis: implications in neovascular age-related macular degeneration and treatment. Angiogenesis. 2021;24(3):583–595. doi:10.1007/s10456-021-09770-0
  • Nakajima K, Higuchi R, Mizusawa K, et al. Association between extremely high high-density lipoprotein-cholesterol and hypertensive retinopathy: results of a cross-sectional study from Kanagawa investigation of total checkup data from the national database-6 (KITCHEN-6). BMJ Open. 2021;11(5):e043677. doi:10.1136/bmjopen-2020-043677
  • Rema M, Srivastava BK, Anitha B, et al. Association of serum lipids with diabetic retinopathy in urban South Indians--the Chennai Urban Rural Epidemiology Study (CURES) Eye Study--2. Diabet Med. 2006;23(9):1029–1036. doi:10.1111/j.1464-5491.2006.01890.x
  • Ezhilvendhan K, Sathiyamoorthy A, Prakash B, et al. Association of dyslipidemia with diabetic retinopathy in type 2 diabetes mellitus patients: a hospital-based study. J Pharm Bioallied Sci. 2021;13(Suppl 2):S1062–S1067. doi:10.4103/jpbs.jpbs_164_21
  • Zhang X, Wang K, Zhu L, et al. Reverse Cholesterol Transport Pathway and Cholesterol Efflux in Diabetic Retinopathy. J Diabetes Res. 2021;2021:8746114. doi:10.1155/2021/8746114
  • Das R, Kerr R, Chakravarthy U, et al. Dyslipidemia and diabetic macular edema: a systematic review and meta-analysis. Ophthalmology. 2015;122(9):1820–1827. doi:10.1016/j.ophtha.2015.05.011
  • Melancia D, Vicente A, Cunha JP, et al. Diabetic choroidopathy: a review of the current literature. Graefes Arch Clin Exp Ophthalmol. 2016;254(8):1453–1461. doi:10.1007/s00417-016-3360-8
  • Yazgan S, Arpaci D, Celik HU, et al. 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;42(7):1039–1047. doi:10.1080/02713683.2016.1264606
  • KDOQI. KDOQI clinical practice guidelines and clinical practice recommendations for diabetes and chronic kidney disease. Am J Kidney Dis. 2007;49(2 Suppl 2):S12–154. doi:10.1053/j.ajkd.2006.12.005
  • Joint Committee for Developing Chinese guidelines on Prevention and Treatment of Dyslipidemia in Adults. 中国成人血脂异常防治指南 [Chinese guidelines on prevention and treatment of dyslipidemia in adults]. Zhonghua Xin Xue Guan Bing Za Zhi. 2007;35(5):390–419. Chinese.
  • Jaddoe VW, de Jonge LL, Hofman A, et al. First trimester fetal growth restriction and cardiovascular risk factors in school age children: population based cohort study. BMJ. 2014;348:g14. doi:10.1136/bmj.g14
  • Kernan WN, Viscoli CM, Brass LM, et al. Phenylpropanolamine and the risk of hemorrhagic stroke. N Engl J Med. 2000;343(25):1826–1832. doi:10.1056/NEJM200012213432501
  • Busik JV. Lipid metabolism dysregulation in diabetic retinopathy. J Lipid Res. 2021;62:100017. doi:10.1194/jlr.TR120000981
  • Fliesler SJ, Florman R, Rapp LM, et al. In vivo biosynthesis of cholesterol in the rat retina. FEBS Lett. 1993;335(2):234–238. doi:10.1016/0014-5793(93)80736-E
  • Fliesler SJ. Retinal degeneration in a rat model of Smith-Lemli-Opitz Syndrome: thinking beyond cholesterol deficiency. Adv Exp Med Biol. 2010;664:481–489.
  • Elner VM. Retinal pigment epithelial acid lipase activity and lipoprotein receptors: effects of dietary omega-3 fatty acids. Trans Am Ophthalmol Soc. 2002;100:301–338.
  • Tserentsoodol N, Sztein J, Campos M, et al. Uptake of cholesterol by the retina occurs primarily via a low density lipoprotein receptor-mediated process. Mol Vis. 2006;12:1306–1318.
  • Fliesler SJ, Bretillon L. The ins and outs of cholesterol in the vertebrate retina. J Lipid Res. 2010;51(12):3399–3413. doi:10.1194/jlr.R010538
  • Brinks J, van Dijk EHC, Klaassen I, et al. Exploring the choroidal vascular labyrinth and its molecular and structural roles in health and disease. Prog Retin Eye Res. 2021;87:100994. doi:10.1016/j.preteyeres.2021.100994
  • Salazar JJ, Ramírez AI, de Hoz R, et al. Alterations in the choroid in hypercholesterolemic rabbits: reversibility after normalization of cholesterol levels. Exp Eye Res. 2007;84(3):412–422. doi:10.1016/j.exer.2006.10.012
  • Kouchi M, Ueda Y, Horie H, et al. Ocular lesions in Watanabe heritable hyperlipidemic rabbits. Veterinary Ophthalmology. 2006;9(3):145–148. doi:10.1111/j.1463-5224.2006.00453.x
  • Torres RJ, Maia M, Noronha L, et al. Avaliação das alterações precoces na coróide e esclera ocorridas em coelhos hipercolesterolêmicos. Estudo histológico e histomorfométrico [Evaluation of choroid and sclera early alterations in hypercholesterolemic rabbits: histologic and histomorphometric study]. Arq Bras Oftalmol. 2009;72(1):68–74. Portuguese. doi:10.1590/S0004-27492009000100014
  • Ban N, Lee TJ, Sene A, et al. Impaired monocyte cholesterol clearance initiates age-related retinal degeneration and vision loss. JCI Insight. 2018;3(17). doi:10.1172/jci.insight.120824
  • Bhutto IA, Lu Z-Y, Takami Y, et al. Retinal and choroidal vasculature in rats with spontaneous diabetes type 2 treated with the angiotensin-converting enzyme inhibitor cilazapril: corrosion cast and electron-microscopic study. Ophthalmic Res. 2002;34(4):220–231. doi:10.1159/000063877
  • Yang J, Wang E, Zhao X, et al. Optical coherence tomography angiography analysis of the choriocapillary layer in treatment-naïve diabetic eyes. Graefes Arch Clin Exp Ophthalmol. 2019;257(7):1393–1399. doi:10.1007/s00417-019-04326-x
  • Conti FF, Qin VL, Rodrigues EB, et al. Choriocapillaris and retinal vascular plexus density of diabetic eyes using split-spectrum amplitude decorrelation spectral-domain optical coherence tomography angiography. Br J Ophthalmol. 2019;103(4):452–456. doi:10.1136/bjophthalmol-2018-311903
  • Biswas L, Farhan F, Reilly J, et al. TSPO ligands promote cholesterol efflux and suppress oxidative stress and inflammation in choroidal endothelial cells. Int J Mol Sci. 2018;19(12):3740. doi:10.3390/ijms19123740
  • Yeung SC, You Y, Howe KL, et al. Choroidal thickness in patients with cardiovascular disease: a review. Surv Ophthalmol. 2020;65(4):473–486. doi:10.1016/j.survophthal.2019.12.007
  • Alm A, Bill A. Ocular and optic nerve blood flow at normal and increased intraocular pressures in monkeys (Macaca irus): a study with radioactively labelled microspheres including flow determinations in brain and some other tissues. Exp Eye Res. 1973;15(1):15–29. doi:10.1016/0014-4835(73)90185-1
  • Kim JH, Kim S, Kim S, et al. Relationship between coronary artery calcification and central chorioretinal thickness in patients with subclinical atherosclerosis. Ophthalmologica. 2021;244(1):18–26. doi:10.1159/000506056
  • Kocamaz M, Karadağ O, Onder SE. Comparison of choroidal thicknesses in patients with coronary artery disease and patients at risk of coronary artery disease. Int Ophthalmol. 2021;41(6):2117–2124. doi:10.1007/s10792-021-01769-2
  • Ala-Kauhaluoma M, Koskinen SM, Silvennoinen H, et al. Subfoveal choroidal thickness in ipsi- and contralateral eyes of patients with carotid stenosis before and after carotid endarterectomy: a prospective study. Acta Ophthalmol. 2021;99(5):545–552. doi:10.1111/aos.14648
  • Ossoli A, Pavanello C, Giorgio E, et al. Dysfunctional HDL as a therapeutic target for atherosclerosis prevention. Curr Med Chem. 2019;26(9):1610–1630. doi:10.2174/0929867325666180316115726
  • Masuda D, Yamashita S. Very high levels of high-density lipoprotein cholesterol and cardiovascular events in Japanese population. J Atheroscler Thromb. 2016;23(7):771–772. doi:10.5551/jat.ED049
  • Singh K, Rohatgi A. Examining the paradox of high high-density lipoprotein and elevated cardiovascular risk. J Thorac Dis. 2018;10(1):109–112. doi:10.21037/jtd.2017.12.97
  • Madsen CM, Nordestgaard BG. Is it time for new thinking about high-density lipoprotein? Arterioscler Thromb Vasc Biol. 2018;38(3):484–486. doi:10.1161/ATVBAHA.118.310727
  • Burgess S, Davey Smith G. Mendelian randomization implicates high-density lipoprotein cholesterol-associated mechanisms in etiology of age-related macular degeneration. Ophthalmology. 2017;124(8):1165–1174. doi:10.1016/j.ophtha.2017.03.042
  • Wang Y, Wang M, Zhang X, et al. The association between the lipids levels in blood and risk of age-related macular degeneration. Nutrients. 2016;8(10):8.
  • Feng H, Li XA. Dysfunctional high-density lipoprotein. Curr Opin Endocrinol Diabetes Obes. 2009;16(2):156–162. doi:10.1097/MED.0b013e32832922fc
  • Sasso FC, Pafundi PC, Gelso A, et al. High HDL cholesterol: a risk factor for diabetic retinopathy? Findings from NO BLIND study. Diabetes Res Clin Pract. 2019;150:236–244. doi:10.1016/j.diabres.2019.03.028
  • Gupta P, Jing T, Marziliano P, et al. Peripapillary choroidal thickness assessed using automated choroidal segmentation software in an Asian population. Br J Ophthalmol. 2015;99(7):920–926. doi:10.1136/bjophthalmol-2014-306152