Subclinical Signs of Retinal Microvascular Impairment in Obese Patients
DOI:
https://doi.org/10.48560/rspo.25385Keywords:
Fluorescein Angiography, MicrovesselsAbstract
INTRODUCTION: Basic science research has shown that obesity is associated with enhanced oxidative stress, reduced nitric oxide availability and secondary microvascular endothelial dysfunction. However, the clinical demonstration of this microvasculature damage has been chal- lenging because of the in vivo inaccessibility of the small capillaries. This study sought to evaluate the impact of obesity in the structure and microvasculature of the retina using a clinically available non-invasive technology.
METHODS: Obese patients (body mass index, BMI ≥35 kg/m2) with no history of clinically evident microvascular disease and age-matched controls were consecutively recruited. Retina macular structure was evaluated as retinal thickness in the different retinal layers in the foveal, parafoveal and perifoveal regions using optical coherence tomography (OCT). Macular vascular properties were evaluated using OCT angiography. Foveal avascular zone properties and vascular density (in both superior (SVP) and deep vascular plexus (DVP)) were computed. Clinically relevant adjustments were performed.
RESULTS: A total of 79 participants were included (49 obese, 30 age-matched controls). Obese patients had subclinical signs of retinal microvascular impairment when compared to controls (increased retinal foveal avascular zone area and irregularity (area: 0.38±0.12 vs 0.32±0.10 mm2, p=0.037; perimeter: 2.33±0.37 vs 2.08±0.35 mm, p=0.002; circularity: 0.85±0.09 vs 0.91±0.04, p<0.001) and decreased parafoveal vascular density in the DVP (62.4±10.1 vs 67.7±9.8, p=0.020), despite preserved structural retinal layers thickness. These differences were not influenced by the clinical diagnosis of diabetes.
CONCLUSION: Obese patients in our sample had subclinical signs of microvascular impairment when compared to controls. This subclinical retinal microvascular impairment may reflect an initial stage of a systemic microangiopathic process that deserves our attention as obesity prevalence keeps growing worldwide.
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References
World Health Organization. Obesity and overweight - Key facts. Geneva: WHO; 2020.
Virdis A, Masi S, Colucci R, Chiriacò M, Uliana M, Puxeddu I, et al. Microvascular endothelial dysfunction in patients with obesity. Curr Hypertens Rep. 2019;21:32. doi: 10.1007/s11906-019-0930-2.
Afshin A, Forouzanfar MH, Reitsma MB, Sur P, Estep K, Lee A, et al. Health effects of overweight and obesity in 195 countries over 25
years. N Engl J Med. 2017;377:13–27. doi: 10.1056/NEJMoa1614362.
Karaca Ü, Schram MT, Houben AJ, Muris DM, Stehouwer CD. Microvascular dysfunction as a link between obesity, insulin resistance and hypertension. Diabetes Res Clin Pract.
;103:382-7. doi: 10.1016/j.diabres.2013.12.012.
Campia U, Tesauro M, Cardillo C. Human obesity and endotheli-um-dependent responsiveness. Br J Pharmacol. 2012;165:561–73.
Toda N, Okamura T. Obesity impairs vasodilatation and blood flow increase mediated by endothelial nitric oxide: An overview. J Clin Pharmacol. 2013;53:1228–39.
das Graças Coelho de Souza M, Kraemer-Aguiar LG, Bouskela E. Inflammation-induced microvascular dysfunction in obesity - A translational approach. Clin Hemorheol Microcirc.
;64:645-54. doi: 10.3233/CH-168018.
De Jongh RT, Serné EH, Ijzerman RG, De Vries G, Stehouwer CD. Impaired microvascular function in obesity: Implications for obesity-associated microangiopathy, hypertension, and insulin resistance. Circulation. 2004;109:2529–35.
Rossi M, Nannipieri M, Anselmino M, Pesce M, Muscelli E, Santoro G, et al. Skin vasodilator function and vasomotion in patients with morbid obesity: Effects of gastric bypass surgery. Obes Surg. 2011;21:87–94.
Campbell DJ, Somaratne JB, Prior DL, Yii M, Kenny JF, Newcomb AE, et al. Obesity is associated with lower coronary microvascular density. PLoS One. 2013;8:7–9. doi: 10.1371/journal.pone.0081798.
Rodríguez F, Staurenghi G. RG-GA for, 2018 undefined. The role of OCT-A in retinal disease management. Berlin: Springer; 2018.
Gildea D. The diagnostic value of optical coherence tomography angiography in diabetic retinopathy: a systematic review. Int Ophthalmol. 2019;39:2413–33. doi: 10.1007/s10792-018-1034-8.
Tan AC, Tan GS, Denniston AK, Keane PA, Ang M, Milea D, et al. An overview of the clinical applications of optical coherence tomography angiography. Eye. 2018;32:262–86. doi: 10.1038/eye.2017.181.
Tey KY, Teo K, Tan AC, Devarajan K, Tan B, Tan J, et al. Optical coherence tomography angiography in diabetic retinopathy: a review of current applications. Eye Vis. ;6:37. doi: 10.1186/s40662-019-0160-3.
Kashani AH, Chen CL, Gahm JK, Zheng F, Richter GM, Rosenfeld PJ, et al. Optical coherence tomography angiography: A comprehensive review of current methods and clinical applications. Prog Retin Eye Res. 2017;60:66-100. doi: 10.1016/j.preteyeres.2017.07.002.
Laiginhas R, Guimarães M, Cardoso P, Santos-Sousa H, Preto J, Nora M, et al. Retinal nerve fiber layer thickness decrease in obesity as a marker of neurodegeneration. Obes Surg. 2019;29:2174–9. doi: 10.1007/s11695-019-03806-7.
Laiginhas R, Guimarães M, Cardoso P, Santos-Sousa H, Preto J, Nora M, Chibante J, Falcão-Reis F, Falcão M. Bariatric surgery induces retinal thickening without affecting the retinal nerve fiber layer independent of diabetic status. Obes Surg. 2020;30:4877–84. doi: 10.1007/s11695-020-04904-7.
Laiginhas R, Guimarães M, Nora M, Chibante J, Falcão M. Gastric bypass improves microvascular perfusion in patients with obe- sity. Obes Surg. 2021;31:2080-6. doi: 10.1007/s11695-021-05223-1.
American Diabetes Association Professional Practice Com- mittee. 2. Classification and Diagnosis of Diabetes: Standards of Medical Care in Diabetes-2022. Diabetes Care. 2022;45:S17- S38. doi: 10.2337/dc22-S002.
Raman M, Middleton RJ, Kalra PA, Green D. Estimating renal function in old people: an in-depth review. Int Urol Nephrol. 2017;49:1979-88. doi: 10.1007/s11255-017-1682-z.
Rasband WS. ImageJ. Bethesda: U. S. National Institutes of Health; 2018.
Vujosevic S, Toma C, Villani E, Muraca A, Torti E, Florimbi G, et al. Diabetic macular edema with neuroretinal detachment: OCT and OCT-angiography biomarkers of treatment response to anti-VEGF and steroids. Acta Diabetol. 2020;57:287- 96. doi: 10.1007/s00592-019-01424-4.
Stehouwer CD. Microvascular dysfunction and hyperglyce- mia: A vicious cycle with widespread consequences. Diabetes. 2018;67:1729–41.
Muris DM, Houben AJ, Kroon AA, Henry RM, van der Kallen CJ, Sep SJ, et al. Age, waist circumference, and blood pressure are associated with skin microvascular flow motion: the Maastricht Study. J Hypertens. 201432:2439-49; discussion 2449. doi: 10.1097/HJH.0000000000000348.
de Jongh RT, Ijzerman RG, Serné EH, Voordouw JJ, Yudkin JS, de Waal HA, et al. Visceral and truncal subcutaneous adipose tissue are associated with impaired capillary recruitment in healthy individuals. J Clin Endocrinol Metab. 2006;91:5100-6. doi: 10.1210/jc.2006-1103.
Sörensen BM, Houben AJ, Berendschot TT, Schouten JS, Kroon AA, van der Kallen CJ, et al. Prediabetes and Type 2 Diabetes Are Associated With Generalized Microvascular Dysfunction: The Maastricht Study. Circulation. 2016;134:1339-52. doi: 10.1161/CIRCULATIONAHA.116.023446.
Dimitriadis GK, Randeva HS, Miras AD. Microvascular complications after metabolic surgery. Lancet Diabetes Endocrinol. 2017;5:240–1. doi: 10.1016/S2213-8587(17)30042-6.
Forbes JM, Cooper ME. Mechanisms of diabetic complications. Physiol Rev. 2013;93:137–88.
Brownlee M. The pathobiology of diabetic complications: A unifying mechanism. Diabetes. 2005;54:1615–25.
Taqueti VR, Solomon SD, Shah AM, Desai AS, Groarke JD, Osborne MT, et al. Coronary microvascular dysfunction and future risk of heart failure with preserved ejection fraction. Eur Heart J. 2018;39:840–9. doi: 10.1093/eurheartj/ehx721.
Roberts TJ, Burns AT, MacIsaac RJ, MacIsaac AI, Prior DL, Gerche A La. Diagnosis and significance of pulmonary micro-vascular disease in diabetes. Diabetes Care. 2018;41:854–61. doi: 10.2337/dc17-1904.
Weinstein G, Maillard P, Himali JJ, Beiser AS, Au R, Wolf PA, Seshadri S, DeCarli C. Glucose indices are associated with cognitive and structural brain measures in young adults. Neurology. 2015;84:2329–37.
von Scholten BJ, Hasbak P, Christensen TE, Ghotbi AA, Kjaer A, Rossing P, et al. Cardiac 82Rb PET/CT for fast and non-invasive assessment of microvascular function and structure in asymptomatic patients with type 2 diabetes. Diabetologia. 2016;59:371–8.
van Sloten TT, Sedaghat S, Carnethon MR, Launer LJ, Stehouwer CD. Cerebral microvascular complications of type 2 diabetes: stroke, cognitive dysfunction, and depression. Lancet Diabetes Endocrinol. 2020;8:325–36. doi: 10.1016/S2213- 8587(19)30405-X.
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