open access

Vol 74, No 4 (2023)
Original paper
Submitted: 2023-05-23
Accepted: 2023-07-03
Published online: 2023-08-17
Get Citation

Choroidal vascular changes in non-alcoholic fatty liver disease

Enver Avcı1, Ali Kucukoduk2
·
Pubmed: 37823522
·
Endokrynol Pol 2023;74(4):430-436.
Affiliations
  1. Department of Gastroenterology, KTO Karatay Universiy Medical School Medicana Affiliated Hospital, Konya, Turkiye
  2. Department of Ophthalmology, KTO Karatay University Medical School Medicana Affiliated Hospital, Konya, Turkiye

open access

Vol 74, No 4 (2023)
Original Paper
Submitted: 2023-05-23
Accepted: 2023-07-03
Published online: 2023-08-17

Abstract

Introduction: The most common cause of death in nonalcoholic fatty liver disease (NAFLD) is cardiovascular disease. Choroidal microvascular structure in the eye may be a predictor of systemic vascular disease. We aimed to evaluate the effects of NAFLD on the choroidal microvascular structure using enhanced depth optical coherence tomography (EDI-OCT).

Material and methods: This prospective study was conducted by evaluating a total of 96 patients, 52 with steatosis and 44 without steatosis. After anthropometric measurements and ultrasonography were performed in the Gastroenterology Clinic, venous blood samples were taken for biochemical examinations. Then, all patients underwent an eye examination by an ophthalmologist. Subfoveolar choroidal thickness (SFCT) values of the cases were measured with EDI-OCT. Choroid vascular index (CVI) measurements were obtained by dividing the subfoveal choroidal area in the EDI-OCT images into luminal and stromal areas using the image binarization technique (ImageJ). In statistical analysis, the chi-square test was used to compare categorical data, and the independent t-test and Mann-Whitney U test were used to compare quantitative data.

Results: The mean age of those with fatty liver was 41±15.7 years, and of those without fatty liver it was 46 ± 10.7 years. There was no statistically significant difference between the groups in terms of age (p = 0.064). Body mass index (BMI), waist circumference (WC), glucose, uric acid, alanine aminotransferase (ALT), gamma glutamyl transpeptidase (GGT), total cholesterol (TC), ferritin, insulin, and Homestatic Model Assesment — Insuline Restistance (HOMA-IR) were statistically significantly higher in the NAFLD group. On the other hand, there was no statistically significant difference between the groups in terms of low-density lipoprotein (LDL)-cholesterol, high-density lipoprotein (HDL)-cholesterol, triglyceride, and aspartate aminotransferase (AST) values. The mean SFCT was measured as 280.26 ± 23.68 microns in the NAFLD group, and 308.96 ± 18.57 microns in the control group. There was no statistically significant difference in SFCT between the groups (p = 0.077). CVI measurements were 0.63 and 0.65, respectively, and they were significantly lower in the group with NAFLD (p = 0.045).

Conclusions: This is the first study in the literature to compare patients with and without ultrasonographic fatty liver in terms of choroidal vascular changes. We found that the choroidal vascular index decreased in NAFLD. This result proves that NAFLD causes changes at the microvascular level and is a multisystemic disease.

Abstract

Introduction: The most common cause of death in nonalcoholic fatty liver disease (NAFLD) is cardiovascular disease. Choroidal microvascular structure in the eye may be a predictor of systemic vascular disease. We aimed to evaluate the effects of NAFLD on the choroidal microvascular structure using enhanced depth optical coherence tomography (EDI-OCT).

Material and methods: This prospective study was conducted by evaluating a total of 96 patients, 52 with steatosis and 44 without steatosis. After anthropometric measurements and ultrasonography were performed in the Gastroenterology Clinic, venous blood samples were taken for biochemical examinations. Then, all patients underwent an eye examination by an ophthalmologist. Subfoveolar choroidal thickness (SFCT) values of the cases were measured with EDI-OCT. Choroid vascular index (CVI) measurements were obtained by dividing the subfoveal choroidal area in the EDI-OCT images into luminal and stromal areas using the image binarization technique (ImageJ). In statistical analysis, the chi-square test was used to compare categorical data, and the independent t-test and Mann-Whitney U test were used to compare quantitative data.

Results: The mean age of those with fatty liver was 41±15.7 years, and of those without fatty liver it was 46 ± 10.7 years. There was no statistically significant difference between the groups in terms of age (p = 0.064). Body mass index (BMI), waist circumference (WC), glucose, uric acid, alanine aminotransferase (ALT), gamma glutamyl transpeptidase (GGT), total cholesterol (TC), ferritin, insulin, and Homestatic Model Assesment — Insuline Restistance (HOMA-IR) were statistically significantly higher in the NAFLD group. On the other hand, there was no statistically significant difference between the groups in terms of low-density lipoprotein (LDL)-cholesterol, high-density lipoprotein (HDL)-cholesterol, triglyceride, and aspartate aminotransferase (AST) values. The mean SFCT was measured as 280.26 ± 23.68 microns in the NAFLD group, and 308.96 ± 18.57 microns in the control group. There was no statistically significant difference in SFCT between the groups (p = 0.077). CVI measurements were 0.63 and 0.65, respectively, and they were significantly lower in the group with NAFLD (p = 0.045).

Conclusions: This is the first study in the literature to compare patients with and without ultrasonographic fatty liver in terms of choroidal vascular changes. We found that the choroidal vascular index decreased in NAFLD. This result proves that NAFLD causes changes at the microvascular level and is a multisystemic disease.

Get Citation

Keywords

NAFLD; EDI-OCT; choroidal vascular index

About this article
Title

Choroidal vascular changes in non-alcoholic fatty liver disease

Journal

Endokrynologia Polska

Issue

Vol 74, No 4 (2023)

Article type

Original paper

Pages

430-436

Published online

2023-08-17

Page views

789

Article views/downloads

395

DOI

10.5603/ep.95686

Pubmed

37823522

Bibliographic record

Endokrynol Pol 2023;74(4):430-436.

Keywords

NAFLD
EDI-OCT
choroidal vascular index

Authors

Enver Avcı
Ali Kucukoduk

References (43)
  1. Younossi ZM, Koenig AB, Abdelatif D, et al. Global epidemiology of nonalcoholic fatty liver disease-Meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology. 2016; 64(1): 73–84.
  2. Chalasani N, Younossi Z, Lavine JE, et al. The diagnosis and management of nonalcoholic fatty liver disease: Practice guidance from the American Association for the Study of Liver Diseases. Hepatology. 2018; 67(1): 328–357.
  3. European Association for the Study of the Liver (EASL), European Association for the Study of Diabetes (EASD), European Association for the Study of Obesity (EASO). EASL-EASD-EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease. Diabetologia. 2016; 59(6): 1121–1140.
  4. Chalasani N, Younossi Z, Lavine JE, et al. American Gastroenterological Association, American Association for the Study of Liver Diseases, American College of Gastroenterologyh. The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Gastroenterological Association, American Association for the Study of Liver Diseases, and American College of Gastroenterology. Gastroenterology. 2012; 142(7): 1592–1609.
  5. Hashimoto E, Taniai M, Tokushige K. Characteristics and diagnosis of NAFLD/NASH. J Gastroenterol Hepatol. 2013; 28 Suppl 4: 64–70.
  6. Lazo M, Hernaez R, Bonekamp S, et al. Non-alcoholic fatty liver disease and mortality among US adults: prospective cohort study. BMJ. 2011; 343: d6891.
  7. Sinn DH, Kang D, Chang Y, et al. Non-alcoholic fatty liver disease and the incidence of myocardial infarction: A cohort study. J Gastroenterol Hepatol. 2020; 35(5): 833–839.
  8. Yoshitaka H, Hamaguchi M, Kojima T, et al. Nonoverweight nonalcoholic fatty liver disease and incident cardiovascular disease: A post hoc analysis of a cohort study. Medicine (Baltimore). 2017; 96(18): e6712.
  9. Taylor RS, Taylor RJ, Bayliss S, et al. Association Between Fibrosis Stage and Outcomes of Patients With Nonalcoholic Fatty Liver Disease: A Systematic Review and Meta-Analysis. Gastroenterology. 2020; 158(6): 1611–1625.e12.
  10. Imajo K, Hyogo H, Yoneda M, et al. LDL-migration index (LDL-MI), an indicator of small dense low-density lipoprotein (sdLDL), is higher in non-alcoholic steatohepatitis than in non-alcoholic fatty liver: a multicenter cross-sectional study. PLoS One. 2014; 9(12): e115403.
  11. Steiner M, Esteban-Ortega MD, Muñoz-Fernández S. Choroidal and retinal thickness in systemic autoimmune and inflammatory diseases: A review. Surv Ophthalmol. 2019; 64(6): 757–769.
  12. Tan KA, Gupta P, Agarwal A, et al. State of science: Choroidal thickness and systemic health. Surv Ophthalmol. 2016; 61(5): 566–581.
  13. Farrah TE, Dhillon B, Keane PA, et al. The eye, the kidney, and cardiovascular disease: old concepts, better tools, and new horizons. Kidney Int. 2020; 98(2): 323–342.
  14. Keane PA, Sadda SR. Retinal imaging in the twenty-first century: state of the art and future directions. Ophthalmology. 2014; 121(12): 2489–2500.
  15. Agrawal R, Gupta P, Tan KA, et al. Choroidal vascularity index as a measure of vascular status of the choroid: Measurements in healthy eyes from a population-based study. Sci Rep. 2016; 6: 21090.
  16. Wei X, Ting DS, Ng WY, et al. Choroidal Vascularity Index: A Novel Optical Coherence Tomography Based Parameter in Patients With Exudative Age-Related Macular Degeneration. Retina. 2017; 37(6): 1120–1125.
  17. Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985; 28(7): 412–419.
  18. Armstrong MJ, Adams LA, Canbay A, et al. Extrahepatic complications of nonalcoholic fatty liver disease. Hepatology. 2014; 59(3): 1174–1197.
  19. Oni ET, Agatston AS, Blaha MJ, et al. A systematic review: burden and severity of subclinical cardiovascular disease among those with nonalcoholic fatty liver; should we care? Atherosclerosis. 2013; 230(2): 258–267.
  20. Stepanova M, Younossi ZM. Independent association between nonalcoholic fatty liver disease and cardiovascular disease in the US population. Clin Gastroenterol Hepatol. 2012; 10(6): 646–650.
  21. Sinn DH, Kang D, Chang Y, et al. Non-alcoholic fatty liver disease and progression of coronary artery calcium score: a retrospective cohort study. Gut. 2017; 66(2): 323–329.
  22. Kasper P, Martin A, Lang S, et al. NAFLD and cardiovascular diseases: a clinical review. Clin Res Cardiol. 2021; 110(7): 921–937.
  23. Stahl EP, Dhindsa DS, Lee SK, et al. Nonalcoholic Fatty Liver Disease and the Heart: JACC State-of-the-Art Review. J Am Coll Cardiol. 2019; 73(8): 948–963.
  24. Medina-Santillán R, López-Velázquez JA, Chávez-Tapia N, et al. Hepatic manifestations of metabolic syndrome. Diabetes Metab Res Rev. 2013 [Epub ahead of print].
  25. Choudhury J, Sanyal AJ. Insulin resistance and the pathogenesis of nonalcoholic fatty liver disease. Clin Liver Dis. 2004; 8(3): 575–94, ix.
  26. Bugianesi E, McCullough AJ, Marchesini G. Insulin resistance: a metabolic pathway to chronic liver disease. Hepatology. 2005; 42(5): 987–1000.
  27. Friedman SL, Neuschwander-Tetri BA, Rinella M, et al. Mechanisms of NAFLD development and therapeutic strategies. Nat Med. 2018; 24(7): 908–922.
  28. Francque SM, van der Graaff D, Kwanten WJ. Non-alcoholic fatty liver disease and cardiovascular risk: Pathophysiological mechanisms and implications. J Hepatol. 2016; 65(2): 425–443.
  29. Borén J, Chapman MJ, Krauss RM, et al. Low-density lipoproteins cause atherosclerotic cardiovascular disease: pathophysiological, genetic, and therapeutic insights: a consensus statement from the European Atherosclerosis Society Consensus Panel. Eur Heart J. 2020; 41(24): 2313–2330.
  30. Petersen MC, Shulman GI. Mechanisms of Insulin Action and Insulin Resistance. Physiol Rev. 2018; 98(4): 2133–2223.
  31. Tavakol M, Ashraf S, Brener SJ. Risks and complications of coronary angiography: a comprehensive review. Glob J Health Sci. 2012; 4(1): 65–93.
  32. Mushenkova NV, Summerhill VI, Zhang D, et al. Current Advances in the Diagnostic Imaging of Atherosclerosis: Insights into the Pathophysiology of Vulnerable Plaque. Int J Mol Sci. 2020; 21(8).
  33. Kirin M, Nagy R, MacGillivray TJ, et al. Determinants of retinal microvascular features and their relationships in two European populations. J Hypertens. 2017; 35(8): 1646–1659.
  34. Hayreh SS. The blood supply of the optic nerve head and the evaluation of it - myth and reality. Prog Retin Eye Res. 2001; 20(5): 563–593.
  35. Liew G, Wang JJ, Mitchell P, et al. Retinal vascular imaging: a new tool in microvascular disease research. Circ Cardiovasc Imaging. 2008; 1(2): 156–161.
  36. Matulevičiūtė I, Sidaraitė A, Tatarūnas V, et al. Retinal and Choroidal Thinning-A Predictor of Coronary Artery Occlusion? Diagnostics (Basel). 2022; 12(8).
  37. 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.
  38. 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 (Lond). 2020; 34(11): 2068–2075.
  39. Matsuoka S, Kaneko H, Okada A, et al. Association of retinal atherosclerosis assessed using Keith-Wagener-Barker system with incident heart failure and other atherosclerotic cardiovascular disease: Analysis of 319,501 individuals from the general population. Atherosclerosis. 2022; 348: 68–74.
  40. Li S, Lang X, Wang W, et al. Choroidal vascular changes in internal carotid artery stenosis: a retrospective cohort study in Chinese population. BMC Ophthalmol. 2019; 19(1): 215.
  41. Aşıkgarip 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.
  42. 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.
  43. Seo WW, Yoo HS, Kim YD, et al. Choroidal vascularity index of patients with coronary artery disease. Sci Rep. 2022; 12(1): 3036.

Regulations

Important: This website uses cookies. More >>

The cookies allow us to identify your computer and find out details about your last visit. They remembering whether you've visited the site before, so that you remain logged in - or to help us work out how many new website visitors we get each month. Most internet browsers accept cookies automatically, but you can change the settings of your browser to erase cookies or prevent automatic acceptance if you prefer.

Via MedicaWydawcą jest  VM Media Group sp. z o.o., Grupa Via Medica, ul. Świętokrzyska 73, 80–180 Gdańsk

tel.:+48 58 320 94 94, faks:+48 58 320 94 60, e-mail:  viamedica@viamedica.pl