Abstract
Neurocognitive functions develop rapidly in early childhood and depend on the intrinsic cooperation between cerebral structures and the circulatory system. The retinal microvasculature can be regarded as a mirror image of the cerebrovascular circulation. To investigate the association between retinal vessel characteristics and neurological functioning in children aged 4 to 5 years. In this cohort study, mother-child pairs were recruited at birth from February 10, 2010, to June 24, 2014, and renewed consent at their follow-up visit from December 10, 2014, to July 13, 2018. Participants were followed up longitudinally within the prospective Environmental Influence on Aging in Early Life birth cohort. A total of 251 children underwent assessment for this study. Data were analyzed from July 17 to October 30, 2019. Retinal vascular diameters, the central retinal arteriolar equivalent (CRAE), central retinal venular equivalent (CRVE), vessel tortuosity, and fractal dimensions were determined. Attention and psychomotor speed, visuospatial working memory, and short-term visual recognition memory were assessed by the Cambridge Neuropsychological Test Automated Battery, including the following tasks: Motor Screening (MOT), Big/Little Circle (BLC), Spatial Span (SSP), and Delayed Matching to Sample (DMS). Among the 251 children included in the assessment (135 girls [53.8%]; mean [SD] age, 4.5 [0.4] years), for every 1-SD widening in CRVE, the children performed relatively 2.74% (95% CI, -0.12 to 5.49; P = .06) slower on the MOT test, had 1.76% (95% CI, -3.53% to -0.04%; P = .04) fewer correct DMS assessments in total, and made 2.94% (95% CI, 0.39 to 5.29; P = .02) more errors given a previous correct answer in the DMS task on multiple linear regression modeling. For every 1-SD widening in CRAE, the total percentage of errors and errors given previous correct answers in the DMS task increased 1.44% (95% CI, -3.25% to 0.29%; P = .09) and 2.30% (95% CI, -0.14% to 4.61%; P = .07), respectively. A 1-SD higher vessel tortuosity showed a 4.32% relative increase in latency in DMS task performance (95% CI, -0.48% to 9.12%; P = .07). Retinal vessel characteristics were not associated with BLC and SSP test outcomes. These findings suggest that children's microvascular phenotypes are associated with short-term memory and that changes in the retinal microvasculature may reflect neurological development during early childhood.
Highlights
Neurological development is at its most crucial phase during early childhood
Among the 251 children included in the assessment (135 girls [53.8%]; mean [SD] age, 4.5 [0.4] years), for every 1-SD widening in central retinal venular equivalent (CRVE), the children performed relatively 2.74% slower on the Motor Screening (MOT) test, had 1.76% fewer correct Delayed Matching to Sample (DMS) assessments in total, and made 2.94% more errors given a previous correct answer in the DMS task on multiple linear regression modeling
For every 1-SD widening in central retinal arteriolar equivalent (CRAE), the total percentage of errors and errors given previous correct answers in the DMS task increased 1.44% and 2.30%, respectively
Summary
Important brain structures are formed and reshaped, and dendritic connections of neuronal networks are constantly established until about 5 years of age.[1] Cognitive performance depends on properly functioning cerebral blood circulation, because this part of the vascular network entails approximately 15% of the total human cardiovascular output.[2] Various studies have shown that failure to maintain good cardiovascular health from a young age onward results in a lower scoring of numerous neurological outcomes later in life, such as psychomotor speed, executive function, and verbal memory.[3,4]. The retinal microvasculature can be considered as a proxy of the conditions of the blood vessels in the brain.[7] Structural changes in the retinal vasculature can be early markers for the development of cerebral vascular disease.[8,9] In previous research,[10] smaller retinal arteriolar calibers, summarized as the central retinal arteriolar equivalent (CRAE), have been linked to a lower IQ score in children aged 11 years. To date, retinal vessel diameters and other metrics, such as tortuosity, have never been studied in association with neurocognitive functioning in children as young as 4 years
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