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Can pulsatile CSF flow across the cerebral aqueduct cause ventriculomegaly?: A prospective study of patients with communicating hydrocephalus.
Umeå University, Faculty of Medicine, Department of Radiation Sciences.ORCID iD: 0000-0002-1141-5143
Umeå University, Faculty of Medicine, Department of Radiation Sciences.
Umeå University, Faculty of Medicine, Department of Pharmacology and Clinical Neuroscience, Clinical Neuroscience.ORCID iD: 0000-0001-6451-1940
Umeå University, Faculty of Medicine, Department of Radiation Sciences. Umeå University, Faculty of Medicine, Umeå Centre for Functional Brain Imaging (UFBI).
2019 (English)In: Fluids and Barriers of the CNS, ISSN 2045-8118, E-ISSN 2045-8118, Vol. 16, no 1, article id 40Article in journal (Refereed) Published
Abstract [en]

Background: Communicating hydrocephalus is a disease where the cerebral ventricles are enlarged. It is characterized by the absence of detectable cerebrospinal fluid (CSF) outflow obstructions and often with increased CSF pulsatility measured in the cerebral aqueduct (CA). We hypothesize that the cardiac-related pulsatile flow over the CA, with fast systolic outflow and slow diastolic inflow, can generate net pressure effects that could source the ventriculomegaly in these patients. This would require a non-zero cardiac cycle averaged net pressure difference (ΔPnet) over the CA, with higher average pressure in the lateral and third ventricles.

Methods: We tested the hypothesis by calculating ΔPnet across the CA using computational fluid dynamics based on prospectively collected high-resolution structural (FIESTA-C, resolution 0.39 × 0.39 × 0.3 mm3) and velocimetric (2D-PCMRI, in-plane resolution 0.35 × 0.35 mm2) MRI-data from 30 patients investigated for communicating hydrocephalus.

Results: The ΔPnet due to CSF pulsations was non-zero for the study group (p = 0.03) with a magnitude of 0.2 ± 0.4 Pa (0.001 ± 0.003 mmHg), with higher pressure in the third ventricle. The maximum pressure difference over the cardiac cycle ΔPmax was 20.3 ± 11.8 Pa and occurred during systole. A generalized linear model verified an association between ΔPnet and CA cross-sectional area (p = 0.01) and flow asymmetry, described by the ratio of maximum inflow/outflow (p = 0.04), but not for aqueductal stroke volume (p = 0.35).

Conclusions: The results supported the hypothesis with respect to the direction of ΔPnet, although the magnitude was low. Thus, although the pulsations may generate a pressure difference across the CA it is likely too small to explain the ventriculomegaly in communicating hydrocephalus.

Place, publisher, year, edition, pages
BioMed Central, 2019. Vol. 16, no 1, article id 40
Keywords [en]
Communicating hydrocephalus, computational fluid dynamics, cerebrospinal fluid pressure, brain imaging, cerebral aqueduct
National Category
Medical Engineering
Identifiers
URN: urn:nbn:se:umu:diva-157029DOI: 10.1186/s12987-019-0159-0ISI: 000504082400001PubMedID: 31865917OAI: oai:DiVA.org:umu-157029DiVA, id: diva2:1294052
Funder
Swedish National Space BoardSwedish Research Council, grant 2015-05616Swedish Heart Lung Foundation, grant 20140592
Note

Originally included in thesis in manuscript form

Available from: 2019-03-06 Created: 2019-03-06 Last updated: 2020-01-09Bibliographically approved
In thesis
1. Fluid dynamic principles for analysis of intracranial pressure control: application towards space medicine and hydrocephalus
Open this publication in new window or tab >>Fluid dynamic principles for analysis of intracranial pressure control: application towards space medicine and hydrocephalus
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Alternative title[sv]
Fluiddynamiska principer för analys av intrakraniellt tryck och dess reglering : för tillämpning inom rymdmedicin och hydrocefalus
Abstract [en]

Intracranial pressure (ICP) is an important component of the fluid dynamic environment of the brain and plays a central role with regards to the maintenance of normal cerebral blood flow and neuronal function. However, many regulatory mechanisms controlling the ICP are still poorly understood. One major gap in knowledge in this regard is the mechanism behind the postural/gravitational control of ICP. This is partly due to the fact that most ICP investigations are performed with the patients in a supine or recumbent position. Since most people spend 16 hours a day in an upright position, understanding these mechanics is highly motivated. Also spurring research on this topic is the increasing number of reports of the spaceflight-associated neuro-ocular syndrome (SANS) found in astronauts after prolonged exposure to weightlessness (i.e. microgravity), where evidence suggests that a disrupted balance between ICP and intraocular pressure (IOP) may be an underlying cause. Understanding how ICP is regulated with respect to posture could therefore provide important insight into the alterations introduced by microgravity, where postural effects are removed, and how to improve the safety of astronauts who are susceptible to this syndrome. Here on earth, disturbances in the ICP or cerebrospinal fluid (CSF) dynamics are associated with the development of chronic neurological diseases. One particular disease of interest is communicating hydrocephalus, where the cerebral ventricles are enlarged despite the absence of macroscopic CSF flow obstructions. A common finding in these patients is that of altered pulsatile flow in the CSF. The overall aim of this thesis was to utilize fluid dynamic principles to describe and validate potential regulatory mechanisms behind postural changes in ICP and causes of ventriculomegaly. The thesis is based on four scientific papers (paper I—IV).

A postural dependency of the IOP-ICP pressure difference was verified by simultaneous measurements of ICP (assessed through lumbar puncture) and IOP (measured with an Applanation Resonance Tonometer) (paper I). Based on these measurements, a 24-hour average of the IOP-ICP pressure difference at the level of the eye was estimated for the state of microgravity, predicting a reduced pressure difference in space compared with that on earth.

A hypothesis where postural changes in ICP are described by hydrostatic effects in the venous system, and where these effects are altered by the collapse of the internal jugular veins (IJVs) in more upright positions, was evaluated (paper II and III). Using ultrasound data, it was shown that the venous hydrostatic pressure gradient was balanced by viscous pressure losses in the collapsed IJVs to uphold a near atmospheric pressure at the level of the neck in the upright posture (paper II). A full evaluation of the hypothesis was then performed, based on simultaneous assessment of ICP, central venous pressure (through a PICC-line) and venous collapse in 7 postures of upper-body tilt in healthy volunteers (paper III).The proposed description could accurately predict the general changes seen in the measured ICP for all investigated postures (mean difference: -0.03±2.7 mmHg or -4.0±360 Pa).

Pulsatile CSF flow-induced pressure differences between the ventricles and subarachnoid space were evaluated as a source for ventriculomegaly in communicating hydrocephalus (paper IV). The pressure distributions resulting from the pulsatile CSF flow were calculated using computational fluid dynamics based on MRI data. The estimated pressures revealed a net pressure difference (mean: 0.001±0.003 mmHg or 0.2±0.4 Pa, p=0.03) between the ventricles and the subarachnoid space, over the cardiac cycle, with higher pressure in the third and lateral ventricles.

In conclusion, the results of this thesis support venous hydrostatics and jugular venous collapse as key governing factors in the postural/gravitational control of ICP. Furthermore, a postural dependency of the IOP-ICP pressure difference was demonstrated, providing a potential explanation for how an imbalance between the pressure of the eye and brain can be introduced in microgravity. Computational fluid dynamic analysis revealed that the altered pulsations in communicating hydrocephalus generate a pressure gradient within the CSF system. However, the gradient was small and additional effects are probably needed to explain the ventriculomegaly in these patients. 

Place, publisher, year, edition, pages
Umeå: Umeå Universitet, 2019. p. 67
Series
Umeå University medical dissertations, ISSN 0346-6612 ; 2018
Keywords
Intracranial pressure, posture, cerebrospinal fluid, microgravity, venous collapse, internal jugular vein, fluid dynamics, venous pressure, spaceflight-associated neuro-ocular syndrome, hydrocephalus, mathematical modeling, ultrasound, magnetic resonance imaging
National Category
Physiology
Identifiers
urn:nbn:se:umu:diva-157031 (URN)978-91-7855-029-6 (ISBN)
Public defence
2019-03-29, Hörsal B, Unod T9, Norrlands Universitetssjukhus, Umeå, 13:00 (English)
Opponent
Supervisors
Funder
Swedish National Space BoardSwedish Research Council, grant 2015-05616Swedish Heart Lung Foundation, grant 20140592
Available from: 2019-03-08 Created: 2019-03-06 Last updated: 2019-11-19Bibliographically approved

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Holmlund, PetterQvarlander, SaraMalm, JanEklund, Anders

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