Elsevier

Neurobiology of Aging

Volume 79, July 2019, Pages 59-65
Neurobiology of Aging

Regular article
Quantitative assessment of the intracranial vasculature in an older adult population using iCafe

https://doi.org/10.1016/j.neurobiolaging.2019.02.027Get rights and content

Highlights

  • Increase in age was negatively associated with number of branches and average order.

  • Increase in age was positively associated with average tortuosity.

  • Vascular regions may have different age-related changes for some features.

  • Time-of-flight magnetic resonance angiography and IntraCranial artery feature extraction technique may provide a novel way to assess vascular condition and changes.

Abstract

Comprehensive quantification of intracranial artery features may help us assess and understand variations of blood supply during brain development and aging. We analyzed vasculature features of 163 participants (age 56–85 years, mean of 71) from a community study to investigate if any of the features varied with age. Three-dimensional time-of-flight magnetic resonance angiography images of these participants were processed in IntraCranial artery feature extraction technique (a recently developed technique to obtain quantitative features of arteries) to divide intracranial vasculatures into anatomical segments and generate 8 morphometry and intensity features for each segment. Overall, increase in age was found negatively associated with number of branches and average order of intracranial arteries while positively associated with tortuosity, which remained after adjusting for cardiovascular risk factors. The associations with number of branches and average order were consistently found between 3 main intracranial artery regions, whereas the association with tortuosity appeared to be present only in middle cerebral artery/distal arteries. The combination of time-of-flight magnetic resonance angiography and IntraCranial artery feature extraction technique may provide an effective way to study vascular conditions and changes in the aging brain.

Introduction

Older age is a major risk factor for cardiovascular disease and is associated with a number of deleterious changes in the cardiovascular system, such as coronary disease, hypertension, congestive heart failure, and stroke (Lakatta and Levy, 2003, Najjar et al., 2005). Age-specific mortality rates from heart disease and stroke increase exponentially with age throughout the later years of life, accounting for more than 40% of all deaths among people aged 65–74 years and almost 60% at age 85 years and older (Ungvari et al., 2010).

Various vascular changes with normal aging have been explored, especially in the older adult population. Previous studies have identified microvascular and macrovascular changes associated with aging, including decreased microvascular density (Brown and Thore, 2011), loss of microvascular plasticity (Riddle et al., 2003), progressive luminal dilation (Gutierrez et al., 2016), increased vessel tortuosity (Kamenskiy et al., 2015), and vessel wall thickening (Farkas et al., 2006). In addition to arterial structural changes, unsurprisingly, aging has also been shown to lead to significant changes in cerebral vascular flow (Kalaria, 1996, Kety, 1955, Scheinberg et al., 1953). Quantifiable from three-dimensional time-of-flight (TOF) magnetic resonance angiography (MRA) (Bullitt et al., 2003, Bullitt et al., 2009, Wright et al., 2013), brain arterial maps can be generated to reflect the vascular supply of the brain (Bernier et al., 2018, Viviani, 2016), and these physiological and pathophysiological changes in cerebral vasculature are believed to be implicated in the pathogenesis of many common neurological diseases such as stroke and Alzheimer's disease (Arvanitakis et al., 2016, Webster et al., 1995, Yonas et al., 1993).

However, the lack of appropriate quantitative image analysis tools and insufficient data limit studies of cerebral vascular flow and structure changes in the older adults. Most processing techniques are limited to simple structural characterization (number, average radius, and tortuosity) of only a portion of the cerebral arterial tree, thus may miss some global and regional changes in intracranial vasculature. Comprehensive TOF MRA analysis may detect subtle regional vascular changes with aging but has not yet been performed in a large cohort of older adult population. Thus, a comprehensive analysis approach that can quantify vascular features at both global and subregional levels is needed to better understand these relationships between the vascular changes and aging.

IntraCranial artery feature extraction technique (iCafe) (Chen et al., 2018a, Chen et al., 2018b) is a recently developed and validated technique that can evaluate morphometry and intensity features of all vascular regions identified in the brain from TOF MRA images. A reproducibility evaluation of iCafe demonstrated that intracranial artery features quantified by iCafe had good to excellent interscan and intraoperator/interoperator reproducibility (Chen et al., 2018b). With this semiautomated analysis method, each visible artery can be digitally reconstructed with centerline, radius, intensity and artery name available, providing an opportunity to quantify structural and flow-related changes in each possible vasculature territory.

In this study, we used iCafe to comprehensively quantify intracranial vascular features in a cohort of 163 older adults from a community in China to explore their relationships with aging.

Section snippets

Study population

Three-dimensional TOF MRA of 163 participants (age 56–85 years old, mean and standard deviation of 71.6±5.9 years, 74 males) from a pilot community study in China, Cardiovascular Risk of Older Population (Cai et al., 2017, Han et al., 2018, Huang et al., 2017a, Huang et al., 2016, Huang et al., 2017b, Jiang et al., 2015, Qiao et al., 2016, Zhou et al., 2016), was analyzed. All participants with intracranial TOF MRA and clinical information available were selected for analysis from this study.

Results

The clinical characteristics of the study cohort are shown in Table 1. More than half were female (55%). Age ranged from 56 to 85 years (median: 71 years). Cardiovascular risk factors were common, with the Framingham 10-year cardiovascular risk score ≥20% in 40% of the study cohort. Vascular features are summarized in Table 2 for all arteries and separate territories of interest.

The associations between overall vascular features and age are shown in Table 3 and Fig. 2. Aggregated across all

Discussion

In this cross-sectional study, complete intracranial arterial maps were reconstructed, and comprehensive vascular features were extracted using a novel intracranial artery tracing and feature extraction technique. With this comprehensive feature extraction tool, we found that increase in age was associated with fewer branches, a lower average order, and higher tortuosity in the intracranial vasculature. The relationships of age with number of branch and average order were found in all 3 major

Conclusion

Using the intracranial artery feature extraction technique (iCafe), we found that older age was associated with reduced visibility of vascularity of distal arteries as reflected by quantitative measurements of the number of branches, average artery order, and average tortuosity in a large cohort of older adults. iCafe is a novel postprocessing approach for analyzing cerebral vascular health and may provide useful insights for further research on structural and flow-related changes with aging or

Disclosure

The authors have no conflicts of interest to disclose.

Acknowledgements

This research is supported by grants from the National Institutes of Health (R01-NS083503, R01-NS092207, R01-HL103609), National Natural Science Foundation of China (81771825), and Philips Healthcare.

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