Subclinical atherosclerosis associates with diabetic retinopathy incidence: a prospective study.

Publisher: Springer Verlag Country of Publication: Germany NLM ID: 9200299 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1432-5233 (Electronic) Linking ISSN: 09405429 NLM ISO Abbreviation: Acta Diabetol Subsets: MEDLINE

Publication: Berlin : Springer Verlag
Original Publication: Berlin : Springer International, c1991-

Atherosclerosis*/complications ; Atherosclerosis*/epidemiology ; Diabetes Mellitus, Type 2*/complications ; Diabetes Mellitus, Type 2*/epidemiology ; Diabetic Retinopathy*/diagnosis ; Diabetic Retinopathy*/epidemiology ; Diabetic Retinopathy*/etiology; Ankle Brachial Index/adverse effects ; Humans ; Prospective Studies ; Pulse Wave Analysis/adverse effects ; Risk Factors

Background: The prospective correlation between subclinical atherosclerosis and diabetic retinopathy (DR) incidence in Chinese patients with type 2 diabetes mellitus (T2DM) remains elusive.
Methods: Prospective data were obtained from 2781 patients with diabetes, among whom 1,964 and 2,180 T2DM patients without any and referable DR at baseline, respectively, were included in the analysis. Multivariate analyses were performed using the Cox proportional hazards model.
Results: Over a median follow-up of 22.2 months (interquartile range 12.7-27.7), 282 (14.36%) and 125 (5.73%) patients developed any and referable DR, respectively. After adjustment for confounders, each standard deviation (SD) increase in brachial-ankle pulse wave velocity (ba-PWV) was associated with 31% (95% confidence interval 1.15-1.50) and 38% (1.14-1.66) higher risks of incident any and referable DR, respectively. Compared with the lowest ba-PWV quartile, the highest ba-PWV quartile had 135% (1.48-3.72) and 293% (1.83-8.44) higher risks of developing any and referable DR, respectively. Per SD increase of pulse pressure (PP) was associated with 22% (1.09-1.38) and 22% (1.02-1.46) higher risks of incident any and referable DR, respectively. The restricted cubic spline models further indicated a significant linear association of baseline subclinical atherosclerosis with referable DR, and a nonlinear association with any DR. In addition, adding the ba-PWV to the prognostic model for DR incidence improved the C-statistic value, the integrated discrimination improvement value, and the net reclassification improvement value (all P < 0.05).
Conclusions: Baseline subclinical atherosclerosis was significantly associated with an increased risk of DR incidence, and elevated ba-PWV independently predicted incident DR in T2DM patients.
(© 2022. Springer-Verlag Italia S.r.l., part of Springer Nature.)

Cho NH, Shaw JE, Karuranga et al. (2018) IDF Diabetes atlas: global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract 138:271–281. (PMID: 10.1016/j.diabres.2018.02.023)
Sabanayagam C, Banu R, Chee ML et al. (2019) Incidence and progression of diabetic retinopathy: a systematic review. Lancet Diabetes Endocrinol 7(2):140–149. (PMID: 10.1016/S2213-8587(18)30128-1)
Ikram MK, Cheung CY, Lorenzi M, Klein R, Jones TL, Wong TY (2013) NJWoRBfD group retinal vascular caliber as a biomarker for diabetes microvascular complications. Diabetes Care 36(3):750–759. (PMID: 10.2337/dc12-1554)
Manon V Van Hecke, Jacqueline M Dekker, Giel Nijpels et al. (2003) Retinopathy is associated with cardiovascular and all-cause mortality in both diabetic and nondiabetic subjects: the hoorn study. Diabetes Care 2610(10):2958.
Kristensen SL, Rorth R, Jhund PS et al. (2018) Microvascular complications in diabetes patients with heart failure and reduced ejection fraction-insights from the beta-blocker evaluation of survival trial. Eur J Heart Fail 20(11):1549–1556. (PMID: 10.1002/ejhf.1201)
Cheung N, Rogers S, Couper DJ, Klein R, Sharrett AR, Wong TY (2007) Is diabetic retinopathy an independent risk factor for ischemic stroke? Stroke 38(2):398–401. (PMID: 10.1161/01.STR.0000254547.91276.50)
Juutilainen A, Lehto S, Ronnemaa T, Pyorala K, Laakso M (2007) Retinopathy predicts cardiovascular mortality in type 2 diabetic men and women. Diabetes Care 30(2):292–299. (PMID: 10.2337/dc06-1747)
Martinez-Lopez D, Roldan-Montero R, Garcia-Marques F et al. (2020) Complement C5 protein as a marker of subclinical atherosclerosis. J Am Coll Cardiol 75(16):1926–1941. (PMID: 10.1016/j.jacc.2020.02.058)
Fernandez-Friera L, Penalvo JL, Fernandez-Ortiz A et al. (2015) Prevalence, vascular distribution, and multiterritorial extent of subclinical atherosclerosis in a middle-aged cohort: the PESA (progression of early subclinical atherosclerosis) study. Circulation 131(24):2104–2113. (PMID: 10.1161/CIRCULATIONAHA.114.014310)
Theilade S, Lajer M, Persson F, Joergensen C, Rossing P (2013) Arterial stiffness is associated with cardiovascular, renal, retinal, and autonomic disease in type 1 diabetes. Diabetes Care 36(3):715–721. (PMID: 10.2337/dc12-0850)
Liu SC, Chuang SM, Shih HM, Wang CH, Tsai MC et al. (2020) High pulse wave velocity is associated with the severity of diabetic retinopathy in patients with type 2 diabetes. J Investig Med 68(6):1159–1165. (PMID: 10.1136/jim-2019-001240)
Kawasaki R, Cheung N, Islam FM et al. (2011) A multi-ethnic study of Is diabetic retinopathy related to subclinical cardiovascular disease? Ophthalmology 118(5):860–865. (PMID: 10.1016/j.ophtha.2010.08.040)
Steppan J, Barodka V, Berkowitz DE, Nyhan D (2011) Vascular stiffness and increased pulse pressure in the aging cardiovascular system. Cardiol Res Pract 2011:263585. (PMID: 10.4061/2011/263585)
An Y, Yang Y, Cao B et al. (2021) Increased arterial stiffness as a predictor for onset and progression of diabetic retinopathy in type 2 diabetes mellitus. J Diabetes Res 2021:9124656. (PMID: 10.1155/2021/9124656)
Antonopoulos AS, Siasos G, Oikonomou E et al. (2021) Arterial stiffness and microvascular disease in type 2 diabetes. Eur J Clin Invest 51(2):e13380. (PMID: 10.1111/eci.13380)
Zhang Y, Wang W, Ning G (2019) Metabolic management center: an innovation project for the management of metabolic diseases and complications in China. J Diabetes 11(1):11–13. (PMID: 10.1111/1753-0407.12847)
Wang S, Shi J, Peng Y, et al. (2021) Stronger association of triglyceride glucose index than the HOMA-IR with arterial stiffness in patients with type 2 diabetes: a real-world single-centre study. Cardiovasc Diabetol 20(1):82. (PMID: 10.1186/s12933-021-01274-x)
Gabir MM, Hanson RL, Dabelea D et al. (2000) The 1997 american diabetes association and 1999 world health organization criteria for hyperglycemia in the diagnosis and prediction of diabetes. Diabetes Care 23(8):1108–1112. (PMID: 10.2337/diacare.23.8.1108)
Ogawa O, Hiraoka K, Watanabe T, et al. (2008) Diabetic retinopathy is associated with pulse wave velocity, not with the augmentation index of pulse waveform. Cardiovasc Diabetol 7:11. (PMID: 10.1186/1475-2840-7-11)
Ato D (2018) Pitfalls in the ankle-brachial index and brachial-ankle pulse wave velocity. Vasc Health Risk Manag 14:41–62. (PMID: 10.2147/VHRM.S159437)
Cardoso CRL, Melo JV, Santos TRM, Leite NC, Salles GF (2021) Traditional and non-traditional risk factors for peripheral artery disease development/progression in patients with type 2 diabetes: the Rio de Janeiro type 2 diabetes cohort study. Cardiovasc Diabetol 20(1):54. (PMID: 10.1186/s12933-021-01249-y)
Zhang Y, Shi J, Peng Y, et al. (2020) Artificial intelligence-enabled screening for diabetic retinopathy: a real-world multicenter and prospective study. BMJ Open Diabetes Res Care 8(1):001596.
Zhang T, Shi J, Peng Y, et al. (2020) Sex-influenced association between free triiodothyronine levels and poor glycemic control in euthyroid patients with type 2 diabetes mellitus. J Diabetes Complic 34(11):107701. (PMID: 10.1016/j.jdiacomp.2020.107701)
Lin L, Zhang J, Jiang L, et al. (2020) Transition of metabolic phenotypes and risk of subclinical atherosclerosis according to BMI: a prospective study. Diabetologia 63(7):1312–1323. (PMID: 10.1007/s00125-020-05116-5)
Xin Z, Zhu Y, Wang S, et al. (2020) Associations of subclinical atherosclerosis with nonalcoholic fatty liver disease and fibrosis assessed by non-invasive score. Liver Int 40(4):806–814. (PMID: 10.1111/liv.14322)
Wilkinson CP, Ferris FL, Klein RE, et al. (2003) Global diabetic retinopathy project proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology 110(9):1677–1682. (PMID: 10.1016/S0161-6420(03)00475-5)
Natarajan S, Jain A, Krishnan R, Rogye A, Sivaprasad S (2019) Diagnostic accuracy of community-based diabetic retinopathy screening with an offline artificial intelligence system on a smartphone. JAMA Ophthalmol 137(10):1182. (PMID: 10.1001/jamaophthalmol.2019.2923)
Matthews CE, Moore SC, Arem H,et al. (2020) Amount and intensity of leisure-time physical activity and lower cancer risk. J Clin Oncol 38(7):686–697. (PMID: 10.1200/JCO.19.02407)
Ferreira I, Hovind P, Schalkwijk CG, Parving HH, Stehouwer CDA, Rossing P (2018) Biomarkers of inflammation and endothelial dysfunction as predictors of pulse pressure and incident hypertension in type 1 diabetes: a 20 year life-course study in an inception cohort. Diabetologia 61(1):231–241. (PMID: 10.1007/s00125-017-4470-5)
Yamamoto M, Fujihara K, Ishizawa M, et al. (2019) Pulse pressure is a stronger predictor than systolic blood pressure for severe eye diseases in diabetes mellitus. J Am Heart Assoc 8(8):e010627. (PMID: 10.1161/JAHA.118.010627)
Agundez J, Ladero J, Diaz-Rubio M, Benitez J (1996) Rsa I polymorphism at the cytochrome P4502E1 locus is not related to the risk of alcohol-related severe liver disease. Liver 16(6):380–383. (PMID: 10.1111/j.1600-0676.1996.tb00766.x)
Haas AV, McDonnell ME (2018) Pathogenesis of cardiovascular disease in diabetes. Endocrinol Metab Clin North Am 47(1):51–63. (PMID: 10.1016/j.ecl.2017.10.010)
Vistoli G, De Maddis D, Cipak A, Zarkovic N, Carini M, Aldini G (2013) Advanced glycoxidation and lipoxidation end products (AGEs and ALEs): an overview of their mechanisms of formation. Free Radic Res 47(Suppl 1):3–27. (PMID: 10.3109/10715762.2013.815348)
Wolf D, Ley K (2019) Immunity and inflammation in atherosclerosis. Circ Res 124(2):315–327. (PMID: 10.1161/CIRCRESAHA.118.313591)
Back M, Yurdagul A Jr, Tabas I, Oorni K, Kovanen PT (2019) Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities. Nat Rev Cardiol 16(7):389–406. (PMID: 308468756727648)
Ruparelia N, Choudhury R (2020) Inflammation and atherosclerosis: what is on the horizon? Heart 106(1):80–85. (PMID: 10.1136/heartjnl-2018-314230)

DMRFP_II_01 SHMHDF; 2016YFC0901200 National Key Research and Development Program of China; 2018YFC1311800 National Key Research and Development Program of China; 2018YFC1314800 National Key Research and Development Program of China; 2019LJ07 Program of Shanghai Academic Research Leader

Keywords: Brachial-ankle pulse wave velocity; Diabetic retinopathy; Pulse pressure; Subclinical atherosclerosis; Type 2 diabetes mellitus

Date Created: 20220527 Date Completed: 20220701 Latest Revision: 20220701

20231215

10.1007/s00592-022-01897-w

35624320