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Extracranial Versus Intracranial Hydro-Hemodynamics During Aging: a PC-MRI Pilot Cross-Sectional Study

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Extracranial Versus Intracranial Hydro-Hemodynamics During Aging: a PC-MRI Pilot Cross-Sectional Study Lokossou et al. Fluids Barriers CNS (2020) 17:1 https://doi.org/10.1186/s12987-019-0163-4 Fluids and Barriers of the CNS RESEARCH Open Access Extracranial versus intracranial hydro-hemodynamics during aging: a PC-MRI pilot cross-sectional study Armelle Lokossou1* , Serge Metanbou2, Catherine Gondry‑Jouet2 and Olivier Balédent1,3* Abstract Background: Both aging and changes in blood fow velocity between the extracranial (intraspinal) and intracranial regions of cerebral vessels have an impact on brain hydro‑hemodynamics. Arterial and venous cerebral blood fows interact with cerebrospinal fuid (CSF) in the both the cranial and spinal systems. Studies suggest that increased blood and CSF fow pulsatility plays an important role in certain neurological diseases. Here, we investigated the changes in blood‑CSF fow pulsatility in the cranial and spinal systems with age as well as the impact of the intracranial compart‑ ment on fow patterns. Method: Phase‑contrast magnetic resonance imaging (PC‑MRI) was performed in 16 young and 19 elderly healthy volunteers to measure the fows of CSF and blood. CSF stroke volume (SV), blood SV, and arterial and venous pulsatil‑ ity indexes (PIs) were assessed at intra‑ and extracranial levels in both samples. Correlations between ventricular and spinal CSF fow, and between blood and CSF fow during aging were also assessed. Results: There was a signifcant decrease in arterial cerebral blood fow and intracranial venous cerebral blood fow with aging. We also found a signifcant increase of intracranial blood SV, spinal CSF SV and arterial/venous pulsatility indexes with aging. In regard to intracranial compartment impact, arterial and venous PIs decreased signifcantly at intracranial level in elderly volunteers, while young adults exhibited decrease in venous PI only. Intracranial venous PI was paradoxically lower than extracranial venous PI, regardless of age. In both sample groups, spinal CSF SV and aqueductal CSF SV were positively correlated, and so were extracranial blood and spinal CSF SVs. Conclusion: The study demonstrates that aging changes blood fow but preserves blood and CSF interactions. We also showed that many parameters related to blood and CSF fows difer between young and elderly adults. Keywords: CSF fow, Arterial cerebral blood fow, Venous cerebral blood fow, PC‑MRI, Aging, Pulsatility Introduction system. Te brain is contained in the rigid skull and sub- Since the development of Phase Contrast Magnetic Reso- ject to biomechanical constraint. Tis is especially rele- nance Imaging (PC-MRI), it is possible to assess the inter- vant for intracranial pressure (ICP) which needs to be in action between blood and CSF fow in the cranio-spinal physiological range to ensure good brain tissue perfusion. Te Monro-Kellie doctrine states that, at steady state, the intracranial volume (brain, CSF, venous and arte- *Correspondence: [email protected]‑picardie.fr; olivier.baledent@chu‑amiens.fr rial blood) is constant. In contrary, at each cardiac cycle, 1 CHIMERE EA 7516 Research Team for Head & Neck, University of Picardie the brain, is subject to pulsatile arterial infow that leads Jules Verne, CHU Amiens Sud, Bâtiment TEP 1er Étage, Unité de to CSF oscillations and venous drainage which in turn Traitement de l’image Médicale, Avenue René Laënnec, 80054 Amiens, France cause ICP changes [1]. Hence, cranio-spinal pulsatility is Full list of author information is available at the end of the article defned as the change in intracranial volume and pressure © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Lokossou et al. Fluids Barriers CNS (2020) 17:1 Page 2 of 11 that occurs periodically with the cardiac cycle. Invasive cerebral blood and CSF fow patterns and their relation- procedures using ICP monitoring and infusion tests are ship is poorly investigated. used to study CSF dynamics in various conditions [2]. As age infuences arterial fow pulsations, we hypoth- Non-invasive approaches are increasingly used to study esized that age would infuence the venous fow pulsa- cranio-spinal pulsatility [3, 4]. For example, stroke vol- tions and the blood-CSF interactions. Te objective was ume, i.e. the mean volume of fuid that oscillates during to assess the efects of the intracranial compartment and the cardiac cycle, is used to assess blood and CSF pulsatil- age on cranio-spinal fows and their pulsatilities, as well ity between diferent compartments [3]. However, the use as on the interplay between CSF and vascular fows. of aqueductal CSF stroke volume as a diagnostic marker of ICP alteration is still debated. For the vascular system, Materials and methods pulsatility or resistance indexes of cerebral blood fow are Study population used as indirect measures for the biomechanical proper- ties of the vascular tree and blood pressure [5, 6]. In this study, we used both elderly and younger popula- Using PC-MRI, some authors showed increased cere- tions to account for the age variation. Te elderly popu- bral arterial pulsatility with aging [7, 8]. Zarrinkoob et al. lation, defned as Healthy Elderly Volunteers (HEV), further showed that the ratio between the extracranial or consisted of 19 elderly subjects (13 women and 6 men). spinal proximal and the intracranial distal artery pulsatil- Teir mean age was 73 ± 6 years. Tey were all recruited ity indices, called the fow dampening factor, is lower for to the Neurology department of our hospital and exam- older people than for the younger ones [8]. Tese authors ined by a neurologist with 10 years’ of experience to attributed this result to the increasing fow pulsatility exclude seizures, transient neurological defcits, or gait with increasing age, as a result of stifness of the vessels disorders. Exclusion criteria were: cognitive decline (all when elastin is replaced by collagen [8]. In recent studies, subjects underwent a neuropsychological screening with Schubert et al. showed that arterial blood fow pulsatil- a Mini-Mental State Examination [MMSE] and score ity decreases from the distal to proximal part of the ves- greater than 26/30), a relevant cerebral neurological dis- sels and that this reduced pulsatility increased with the ease (cerebrovascular accident, meningoencephalitis, tortuosity of the vessels at the level of the atlas or of the tumor), or relevant cerebrovascular risk factors, except carotid siphon [6, 9]. A study by Stoquart-Elsankari et al. arterial hypertension controlled by medication. Te in healthy young adults showed that jugular venous fow healthy elderly volunteers underwent also magnetic reso- pulsatility is higher than the superior sagittal sinus fow nance imaging (MRI) of the brain to exclude ventricular pulsatility [10]. enlargement. Some studies have also suggested a role for fow pulsa- Te younger population, here called Healthy Young tility in some neurological conditions. Indeed, pulse wave Volunteers (HYV), consisted of 16 healthy young subjects encephalopathy is a term associated with disorders such (9 women and 7 men), who underwent cine phase-con- as Alzheimer’s disease, vascular dementia, and hydro- trast MRI. Teir mean age was 31 ± 7 years. Te exclu- cephalus. Te pulse wave encephalopathy theory states sion criteria were: any neurological, psychiatric or severe that there is an underlying vascular pathophysiology general disease, alcoholism, or abnormalities detected by behind these conditions which is related to the strength a clinical MRI exam. of arterial pulse waves induced in the cranio-spinal cav- Te study was approved by the local ethics review com- ity [11]. Bateman showed an increase of 56% of arterial mittee, and written informed consent was obtained from pulsatility and 70% of sagittal sinus pulsatility in hydro- all subjects. cephalus patients compared to patients with dementia In this paper, HEV was used to designate subjects [12]. El Sankari et al. showed an increase of vascular pul- belonging to the elderly population, and HYV for sub- satility indexes in amnesic patients compared to healthy jects belonging to the young population. subjects [13]. Furthermore, Lim et al. studied the pulsatil- ity of anterior, middle and posterior cerebral arteries and PC‑MRI protocol cognitive functions in patients with middle to moderate All exams were performed using 3T MRI (Signa HDx Alzheimer’s disease. Tey found that the highest values General Electric Medical System, Milwaukee, WI). Te of pulsatility were associated with poor scores after neu- subjects were supine with their head in the 16-channel ropsychology tests and that the rise of these pulsatili- MRI head coil. Sagittal 3D Fiesta (Fast Imaging Employ- ties 1 year after was associated with disease progression ing Steady-state Acquisition) (Fig. 1a) and sagittal 3D [14]. However, to date, unlike the diminution of white phase-contrast angiography (Fig. 2a) were used as ref- and grey matter during physiological aging which is well- erences to set the diferent planes for CSF and blood documented [15, 16], the physiological aging efect on fow acquisitions, respectively.
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