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. 2021 Aug;28(6):e12702.
doi: 10.1111/micc.12702. Epub 2021 May 6.

Carotid stiffness is associated with retinal microvascular dysfunction-The Maastricht study

Frank C T van der Heide  1   2 , Tan Lai Zhou  1   2 , Ronald M A Henry  1   2   3 , Alfons J H M Houben  1   2 , Abraham A Kroon  1   2 , Pieter C Dagnelie  1   2 , Martien C J M van Dongen  4   5 , Simone J P M Eussen  1   5 , Tos T J M Berendschot  6 , Jan S A G Schouten  6   7 , Carroll A B Webers  6 , Miranda T Schram  1   2   3 , Marleen M J van Greevenbroek  1   2 , Anke Wesselius  8 , Casper G Schalkwijk  1   2 , Annemarie Koster  4   9 , Hans H C M Savelberg  10   11 , Nicolaas C Schaper  1   2 , Koen D Reesink  1   3   12 , Coen D A Stehouwer  1   2
Affiliations

Carotid stiffness is associated with retinal microvascular dysfunction-The Maastricht study

Frank C T van der Heide et al. Microcirculation. 2021 Aug.

Abstract

Objective: This study investigated whether arterial stiffening is a determinant of subtle retinal microvascular changes that precede diabetic retinopathy.

Research design and methods: This study used cross-sectional data from the Maastricht Study, a type 2 diabetes-enriched population-based cohort study. We used multivariable linear regression analysis to investigate, in individuals without and with type 2 diabetes, the associations of carotid distensibility coefficient and carotid-femoral pulse wave velocity with retinal microvascular diameters and flicker light-induced dilation and adjusted for cardiovascular and lifestyle risk factors.

Results: The retinal microvascular diameter study population consisted of N = 2434 participants (51.4% men, mean ± SD age 59.8 ± 8.1 years, and 28.1% type 2 diabetes). No measures of arterial stiffness were significantly associated with microvascular diameters. Greater carotid distensibility coefficient (i.e., lower carotid stiffness) was significantly associated with greater retinal arteriolar flicker light-induced dilation (per standard deviation, standardized beta [95% CI] 0.06 [0.00; 0.12]) and non-significantly, but directionally similarly, associated with greater retinal venular flicker light-induced dilation (0.04 [-0.02; 0.10]). Carotid-femoral pulse wave velocity (i.e., aortic stiffness) was not associated with retinal microvascular flicker light-induced dilation. The associations between carotid distensibility coefficient and retinal arteriolar and venular flicker light-induced dilation were two- to threefold stronger in individuals with type 2 diabetes than in those without.

Conclusion: In this population-based study greater carotid, but not aortic, stiffness was associated with worse retinal flicker light-induced dilation and this association was stronger in individuals with type 2 diabetes. Hence, carotid stiffness may be a determinant of retinal microvascular dysfunction.

Keywords: aortic stiffness; arterial stiffness; carotid stiffness; diabetic retinopathy; microvascular dysfunction; retinal microvascular diameter; type 2 diabetes mellitus.

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Conflict of interest statement

No potential conflicts of interest relevant to this article were reported.

Figures

FIGURE 1
FIGURE 1
Retinal microvascular diameter and retinal microvascular flicker light‐induced dilation study population selection
FIGURE 2
FIGURE 2
Associations between carotid DC (per SD) and retinal arteriolar and venular flicker light‐induced dilation (per SD). Standardized regression coefficient (stβ) represents the difference in arteriolar or venular dilation in SD per SD greater carotid DC. In the total population, 1 SD corresponds with 5.14 × 10−3/kPa for carotid DC, 2.82% for flicker light‐induced arteriolar dilation, and 2.20% for flicker light‐induced venular dilation. In participants with type 2 diabetes, 1 SD corresponds with 4.8 × 10−3/kPa for carotid DC, 2.7% for flicker light‐induced arteriolar dilation, and 2.3% for flicker light‐induced venular dilation in participants without diabetes. In participants without diabetes 1 SD corresponds with 5.2 × 10−3/kPa for carotid DC, 2.9% for flicker light‐induced arteriolar dilation, and 2.2% for flicker light‐induced venular dilation. For participants with higher and lower levels of 2‐h PG (≥11.1 mmol/L vs. <11.1), values per SD were quantitatively similar to values per SD for participants with type 2 diabetes and without diabetes, respectively. Variables in model in addition to carotid DC: age, sex, and glucose metabolism status, mean arterial pressure and heart rate, smoking status, alcohol consumption, waist circumference, total‐to‐high density lipoprotein cholesterol ratio, lipid‐modifying and antihypertensive medication, educational status. In stratified analyses, glucose metabolism status was not included in the model. *Indicates statistically significant (p < .05). 2‐h PG, 2‐h post‐load glucose; CI, confidence interval; DC, distensibility coefficient; SD, standard deviation; T2D, type 2 diabetes
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