Is posturerelated craniospinal compliance shift caused by jugular vein collapse? A theoretical analysis
 Manuel Gehlen^{1, 2}Email authorView ORCID ID profile,
 Vartan Kurtcuoglu^{2, 3} and
 Marianne Schmid Daners^{4}
DOI: 10.1186/s1298701700536
© The Author(s) 2017
Received: 9 October 2016
Accepted: 6 February 2017
Published: 16 February 2017
Abstract
Background
Postural changes are related to changes in cerebrospinal fluid (CSF) dynamics. While sitting up leads to a decrease in cranial CSF pressure, it also causes shifts in the craniospinal CSF volume and compliance distribution. We hypothesized that jugular vein collapse in upright posture is a major contributor to these shifts in CSF volume and compliance.
Methods
To test this hypothesis, we implemented a mathematical lumpedparameter model of the CSF system and the relevant parts of the cardiovascular system. In this model, the CSF and the venous system are each divided into a cranial and a spinal part. The pressures in these cranial and spinal portions differ by the posturedependent hydrostatic pressure columns in the connecting vessels. Jugular collapse is represented by a reduction of the hydrostatic pressure difference between cranial and spinal veins. The CSF pressure–volume relationship is implemented as a function of the local CSF to venous pressure gradient. This implies that an increase in CSF volume leads to a simultaneous displacement of blood from adjacent veins. CSF pulsations driven by the cardiovascular system are introduced through a pulsating cranial arterial volume.
Results
In upright posture, the implemented CSF pressure–volume relationship shifts to lower cranial CSF pressures compared to the horizontal position, leading to a decrease in cranial CSF pressure when sitting up. Concurrently, the compliance of the spinal compartment decreases while the one of the cranial compartment increases. With this, in upright posture only 10% of the CSF system’s compliance is provided by the spinal compartment compared to 35% in horizontal posture. This reduction in spinal compliance is accompanied by a caudal shift of CSF volume. Also, the ability of the spinal CSF compartment to compensate for cerebral arterial volume pulsations reduces in upright posture, which in turn reduces the calculated craniospinal CSF flow pulsations.
Conclusion
The mathematical model enabled us to isolate the effect of jugular collapse and quantify the induced shifts of compliance and CSF volume. The good concordance of the modelled changes with clinically observed values indicates that jugular collapse can be considered a major contributor to CSF dynamics in upright posture.
Keywords
Craniospinal Compliance Cerebrospinal fluid dynamics PostureBackground
Several pathologies of the central nervous system, like hydrocephalus and syringomyelia, are caused or characterized by altered cerebrospinal fluid (CSF) dynamics. Therefore, the treatment of these conditions typically aims at restoring physiological circulation of CSF and requires profound knowledge of the underlying pathophysiology. However, CSF dynamics are mostly studied in horizontal posture, even though we spend most of our time upright and CSF dynamics fundamentally change with posture. For example, sitting up not only leads to changes in intracranial pressure (ICP), but also to a caudal shift of CSF volume and an inversion of the compliance distribution between the cranial and the spinal part of the CSF system. This inversion of the craniospinal compliance was first observed by Magnaes in a small number of subjects [1]. In a recent study by Alperin et al. [2], the pulse amplitude of craniospinal CSF flow recorded with magnetic resonance imaging (MRI), decreased in sitting posture, which supports the findings of Magnaes. In CSF shunts, antisiphon devices are used to counteract posturerelated changes in pressures. However, the diversity of functional principles on which these devices are based, indicates that the mechanisms of the posturerelated changes in CSF dynamics and their link to hemodynamics are largely unknown [2]. Knowing the causalities of these interactions would contribute to the understanding of individual pathologies and to the choice of the most appropriate treatment option, especially in the context of various comorbidities typically seen in these patients.
What we do know is that CSF pressure in equilibrium conditions is a function of venous pressure through Davson’s equation [3], and that at least cranial venous pressure changes with posture due to hydrostatic gradients along the blood vessels. Also, cranial venous pressure changes with the state of the jugular veins: when they collapse in upright posture venous resistance increases, reducing both the posturerelated decrease in cranial venous pressure and in CSF pressure [4–6].
We hypothesized that the collapse of the jugular veins when upright not only affects mean ICP, but that it also causes the aforementioned caudal shift of CSF volume: interruption of the venous hydrostatic pressure column decreases the cranial CSF to venous pressure gradient by diminishing the reduction in cranial venous pressure when sitting up. Due to the exponential nature of the CSF system’s pressure–volume relationship [7], this in turn, increases cranial compliance in upright posture. At the same time, the noninterrupted hydrostatic pressure column leads to an increased CSF to venous pressure gradient below the level of the jugular veins, causing the observed caudal shift of CSF volume. Consequently, the spinal dural sac volume increases, reducing the compliance of the spinal CSF space [1].
We aimed at testing this hypothesis by implementing a mathematical model of the CSF system and the relevant parts of the cardiovascular system. This has enabled us to isolate the effect of jugular vein collapse and quantify the induced shifts of compliance and CSF volume. These estimated changes in CSF dynamics were then compared to the measurements of Magnaes [1]. Testing the hypothesis without a mathematical model would be difficult, as jugular collapse can hardly be avoided in vivo. To allow for further model validation, we computed changes in craniospinal CSF flow secondary to changes in craniospinal compliance distribution. Unlike the distribution of compliance itself, changes in CSF flow can be easily measured with MRI and used as surrogate for changes in compliance distribution. With this, we were able to validate the model by comparing the craniospinal flow rates estimated by the model to reported flow rates recorded in supine and sitting posture [2, 8, 9].
Methods
Cerebrospinal fluid pulsations driven by the cardiovascular system were accounted for through a pulsating cranial arterial volume. The pulsations of this arterial volume were based on recorded flow rates in the internal carotid and vertebral arteries. As CSF competes with the arterial pulsations for the available compliance, the arterial volume was added to the cranial CSF volume. Instantaneous flow rates for CSF and venous blood between cranial and spinal compartments were calculated based on a volume balance, assuming constant cranial volume (Monroe–Kelly doctrine).
Model derivation
Local pressure–volume relationships
Parameters, distinctive for normal pressure hydrocephalus
Parameter  Symbol  Value  Unit  Reference 

Elastance  \(E\)  0.23  mL^{−1}  
Exponential parameter  \(p_{1}\)  4  mmHg  [16]* 
Offset pressure  \(p_{0}\)  3.2  mmHg  [16]* 
Rate of CSF formation  \(Q_{form}\)  0.35  mL/min  [13] 
Total CSF outflow resistance  \(R_{abs}^{tot}\)  20.6  mmHg/(mL/min)  
Relative spinal compliance  \(k_{V}\)  0.35  –  [17] 
Spinal venous pressure  \(p_{v}^{s}\)  5.3  mmHg  [4] 
Distance between spinal and cranial reference points  \(l_{sc}\)  33.8  cm  [4] 
Distance between jugular veins and cranial reference point  \(l_{jug}\)  11.0  cm  [4] 
Density of CSF  \(\rho_{CSF}\)  1000  kg/m^{3}  
Density of blood  \(\rho_{blood}\)  1060  kg/m^{3}  
Gravitational acceleration  \(g\)  9.81  m/s^{2}  
Relative spinal outflow conduction  \(k_{R}\)  n/a^{#}  – 
Here, \(k_{V}\) is a constant that describes the portion of the total compensatory reserve of the CSF system attributed to the spinal compartment. In horizontal posture, \(k_{v}\) is the spinal compliance contribution as measured by Magnaes [1].
Hydrostatic pressure gradients
For the spinal part of the model, the hydrostatic indifference point of the venous system was chosen as the reference location. Thus, the spinal venous pressure \(p_{v}^{s}\) was assumed to be independent of posture.
\(l_{jug}\) is the distance between the upper end of the jugular collapse and the reference point of the cranial compartment.
Compliance
CSF formation and absorption
Model parameters
The parameters used for the calculations in this study (Table 1) are characteristic for patients with normal pressure hydrocephalus (NPH). They describe a patient with 12.5 mmHg resting intracranial pressure (\(ICP_{r}\)).
Sensitivity analysis
To analyze the sensitivity of the investigations with respect to the employed parameter values, a three step sensitivity analysis was performed. First, all calculations were repeated with a second parameter set (E = 0.1/mL, p _{1} = 10 mmHg, p _{0} = −5.3 mmHg, \(R_{abs}^{tot} = 13.4\,{\text{mmHg}}/({\text{mL}}/\hbox{min} )\)) that describes physiological CSF dynamics [19]. Second, the parameters determining the hydrostatic gradients within the CSF and the venous system (\(l_{sc}\), \(l_{jug}\), and \(p_{v}^{s}\)) were varied within reported standard deviations (l _{sc} = 33.8 ± 2.5 cm, \(p_{v}^{s} = 5.3 \pm 2.5\, {\text{mmHg}}\)) [4] one at a time. Third, the compliance distribution assumed in horizontal position was varied by ±50% (\(k_{V} = 0.35 \pm 0.175\)).
Cranial arterial volume
Given that arterial pressure is substantially higher than CSF pressure in all but the most extreme pathologic conditions, arterial blood flow rate to the cranium \(Q_{a}\) was assumed unaffected by CSF dynamics. Therefore, the change in cranial arterial volume can be derived from in vivo measurements of \(Q_{a}\). We used flow rates recorded by phasecontrast MRI in the internal carotid and vertebral arteries as arterial blood flow, \(Q_{a}\). These flow rates were obtained from the average of 16 NPH patients [9]. Additionally, the flow rates of a healthy volunteer in supine and sitting position [2] were applied to validate the predicted changes in craniospinal CSF flow.
Evaluation
Sitting up
Upright equilibrium
Simulation of craniospinal flow rates
The CSF volume and the cranial CSF pressure during a cardiac cycle were computed by solving this system of differential–algebraic equations (Eqs. 21, 22) using the Matlab (The MathWorks, Inc., Natick, MA, USA) variableorder solver ‘ode15s’.
Results
After calculating the local and total pressure–volume relationships of the CSF space in horizontal and upright posture, these correlations were used to derive the local and total compliances. Based on this, CSF volume and pressure in upright posture were determined under the assumption of unchanged CSF volume (Eq. 18) or under the assumption of unchanged total compliance (Eq. 19). The posturerelated volume and compliance shifts were then evaluated under these two conditions. Finally, the model output was calculated (Eqs. 21, 22) for one cardiac cycle and the craniospinal flow rates of blood and CSF were derived (Eqs. 23, 24) as a basis for discussion of model validity.
Pressure–volume relationships
Compliance
In Fig. 2b, the local compliances derived analytically from the corresponding pressure–volume relationships (Eqs. 11–14) were plotted along with the combined total compliance for horizontal and upright posture. Similar to the total pressure–volume relationship, the total compliance shifted towards lower cranial CSF pressures in upright posture. Due to a steep increase of the cranial compliance at low CSF pressures, the cranial compartment became the dominant source of compliance at cranial CSF pressures below approximately 0 mmHg.
Posture change
Comparison of CSF pressure, volume and compliance in horizontal and upright posture
Compliance shift
As mentioned before, in upright posture the importance of cranial compliance increased for low CSF pressures. In upright equilibrium, only 10% of the total compliance were provided by the spinal compartment. This corresponded to a 71% reduction relative to the spinal compartment’s contribution in upright posture (Table 2). Under the condition of no change in total CSF volume after sitting up, the total compliance in upright posture strongly increased due to the steep increase in cranial compliance at low CSF pressure. Consequently, the contribution of the spinal compartment towards overall compliance became even lower.
Cerebral CSF pressure (\(p_{CSF}^{c}\)), total, cranial, and spinal change in CSF volume (\(\Delta V^{tot}\), \(\Delta V^{c}\), and \(\Delta V^{s}\)), total compliance (\(C^{tot}\)), and spinal compliance (\(C^{s}\)) in upright posture are shown in comparison to their reference values in horizontal position. The values were calculated under the two alternative assumed conditions of unchanged volume (Eq. 18) and unchanged total compliance (Eq. 19) relative to the horizontal position.
Sensitivity
We analyzed the sensitivity of the reported results to changes in the nominal parameter values (Table 1). This nominal parameter set describes an NPH patient. The physiologic parameter set used to analyze the sensitivity of the model towards changes in the parameters \(E\), \(p_{1}\), \(p_{0}\), and \(R_{abs}^{tot}\) describes a subject with slightly lower CSF pressure in horizontal position. Also, the calculated cranial CSF pressure in upright posture was lower in the physiologic case (−6.6 mmHg after sitting up and −5.9 mmHg in upright equilibrium) compared to the NPH parameter set. The caudal shift of CSF volume caused by sitting up (\(\Delta V^{s}\) in Table 2) was slightly higher (2.1 mL with the physiologic parameter set compared to 1.8 mL in the NPH case). The shift in compliance was not as pronounced as for the NPH parameter set, but the contribution of the spinal compartment to the total compliance still reduced to 18% in upright posture.
For a longer hydrostatic pressure column in the CSF system (l _{ sc } = 36.3 cm), the effect of posture increased as the initial volume shift increased to 2.0 mL (not presented in Table 2), and the contribution of the spinal compliance in upright equilibrium decreased to 7%. Conversely, increased spinal venous pressure \(p_{v}^{s}\) reduced the effect of the jugular vein collapse. Consequently, spinal compliance in upright equilibrium was still 12% and the initial CSF volume shift was reduced to 1.5 mL for 7.7 mmHg spinal venous pressure.
When using different values for the compliance contribution of the spinal compartment in horizontal position (\(k_{V}\)), the caudal shift in CSF volume changed almost proportionally. For example, \(\Delta V^{s}\) reduced to 1.0 mL when \(k_{V}\) was reduced by 50% (\(k_{V} = 0.175\)) and increased to 4.2 mL when \(k_{V}\) was increased by 50% (\(k_{V} = 0.525\)). However, even for such large variations in the compliance distribution (±50%), the reduction of the relative spinal compliance remained between 70 and 82% of its value in horizontal position (\(1 (C^{s} /C^{tot} )/ k_{V}\)).
Patent jugular veins
Without the collapse of the jugular veins (Eq. 7 instead of Eq. 8) only the difference in density can lead to shifts in CSF volume and compliance distribution when changing posture. In this modified model with patent jugular veins in upright posture, 0.4 mL of CSF flowed from the spinal into the cranial compartment when sitting up from horizontal. Cranial CSF pressure in upright posture decreased further (to −13.3 mmHg) with patent jugular veins compared to the case with collapsed jugular veins (−3.3 mmHg).
Cardiac pulsations
In upright posture, this picture changed (Fig. 3, right column). While no change in arterial blood flow was prescribed, craniospinal CSF stroke volume was nevertheless reduced to 10% of the arterial stroke volume (0.2 mL). However, despite these changes in fluid dynamics and changes in absolute pressures, CSF pulse pressure amplitudes remained constant at 1.6 mmHg.
Discussion
Volume and compliance shifts
Our model predicts a posturedependent shift of the craniospinal compliance distribution caused by a caudal displacement of CSF volume. As previously observed by Magnaes [1], this CSF volume displacement in upright posture reduces the compliance provided by the spinal compartment including the spinal thecal sac. It is induced by the hydrostatic pressure column, which is greater in the CSF system compared to the veins, where it is interrupted by the collapsing jugular veins. The estimated shifts of CSF volume and compliance are in range of the observations of Magnaes [1], although he assumed a much higher contribution of the spinal compartment to compliance than in this study [17]. Furthermore, the posturedependent shift of the craniospinal compliance distribution was also observed for large variations of the employed parameter values, indicating that our analysis is robust.
Jugular collapse
Without collapsing jugular veins, the model showed neither a caudal shift of CSF volume nor a cranial shift of the compliance distribution. Furthermore, the fall in cranial CSF pressure was greater than that observed clinically [4, 5]. As jugular collapse reduces this fall in pressure in upright posture, the jugular veins may be seen as serving a protective function for the brain. In hydrocephalus patients with ventriculoperitoneal or ventriculoatrial shunts, this protective mechanism is partially bypassed so that, without appropriate siphon prevention, ICP can decrease to levels as low as those predicted by our model without jugular collapse.
Pressure–volume relationship
The exponential pressure–volume relationship of the CSF system is well proven, at least for normal and reasonably increased CSF pressures (relative to the sagittal sinus pressure). However, for sufficiently decreased CSF volume, it implies infinite compliance. This attribute of the exponential pressure–volume relationship becomes especially problematic when applied to the cranial compliance in upright posture, because negative CSF to venous pressure gradients could easily be reached here. However, as such gradients were not reached in this study this limitation does not affect the results or conclusions reported herein. Nonetheless, extrapolation to low CSF pressures would be invalid (Fig. 2). Therefore, a more accurate description of the pressure–volume relationships would need to be used to study the effect of shunting on CSF dynamics [16, 21].
Only considering the mean venous pressure as counterpressure for the pressure–volume relationship might seem simplistic, as venous pressure varies over the different generations of venous vessels. However, the implemented pressure–volume relationship captures this venous pressure variation and distribution with its exponential shape [22].
The only mechanism of compliance included in the model is the displacement of venous blood. While this mechanism is accepted as the main contributor to compliance in the cranium [10], this is less clear for the rest of the craniospinal space, especially for the spinal thecal sac. However, due to the high distensibility of venous vessels [23], tissue pressure strongly correlates with venous pressure throughout the body. Therefore, it is reasonable to assume that venous pressure is the relevant counterpressure to compliance in the entire CSF system. If the surrounding tissue itself could provide elastic recoil, part of the pressure–volume relation would have to be modelled independent of venous pressure. This would only then decrease the modelled compliance shift, if the elastic tissue were located intracranially, since the counterpressure of the spinal compartment is already assumed to be independent of posture due to its proximity to the venous hydrostatic indifference point [4].
CSF absorption
Before Magnaes [1] determined the craniospinal compliance distribution in some of his patients, similar experiments had been done in adult cats [7]. While in cats the spinal compartment appeared to be less important for compliance, it was still responsible for a significant portion of CSF absorption (16%). Similar proportions of the craniospinal CSF absorption distribution were predicted by our model under the condition of postureindependent total compliance. While this result supports the hypothesis that there is spinal CSF absorption, the exact proportion predicted by the model is sensitive to the employed equilibrium pressure in upright posture. Furthermore, the lengths of hydrostatic pressure columns were calculated based on the assumption of 100% cranial absorption [4]. Taking spinal absorption into account, the estimated value of \(l_{jug}\) would slightly increase, which would decrease the compliance shift predicted by our model.
Craniospinal flows
Pulsatile arterial inflow into the cranium were compensated by simultaneous craniospinal outflow of CSF and venous blood. Stroke volume and amplitude of the calculated CSF pulsations (Figs. 3, 4) were very close to the respective values measured in vivo [2, 8, 9]. Even the reduction in CSF stroke volume was predicted well (Fig. 4). These are strong indications that the increased resistance of the jugular veins in upright posture is responsible for the shift in compliance observed in vivo. Jugular vein collapse can thus be considered a major contributor to CSF dynamics in upright posture. The calculated overall CSF volume hardly changed within a cardiac cycle. Therefore, the ratio of the estimated CSF and the applied arterial stroke volumes was equal to the contribution of the spinal compartment to the overall compliance. In MRI measurements, CSF and even more so the venous pulses are delayed compared to the arterial input. At least some of this delay can be attributed to wave propagation due to vascular distensibility [23]. In the model, these phase shifts between the calculated craniospinal waves were ignored with the implicit assumption of instantaneous transmission of pressures throughout the craniospinal space. However, when assuming that most of the phase shift originates from a wave propagation delay, it does not influence the compliance distribution estimated from the ratio of CSF and arterial stroke volume. In addition to being delayed, recorded venous pulsations appear damped compared to the modelled pulsations. This damping is probably caused by the Windkessel effect in the larger veins, which is not included in our model. However, the craniospinal venous flow rate is not only difficult to model, it is also difficult to measure with MRI as, especially in upright posture it is distributed over numerous small vessels.
Conclusion
Our results support the hypothesis that the jugular veins play an important role in posturerelated changes of CSF dynamics, as their collapse in upright posture induces substantial changes in CSF pressure and compliance.
Abbreviations
 CSF:

cerebrospinal fluid
 ICP:

intracranial pressure
 MRI:

magnetresonance imaging
 NPH:

normal pressure hydrocephalus
Declarations
Authors’ contributions
All authors designed the study and interpreted the data. MG performed the calculations, analyzed the data, and drafted the manuscript. VK and MSD critically revised the manuscript. All authors read and approved the final manuscript.
Acknowledgements
None.
Competing interests
The authors declare that they have no competing interests.
Availability of data and materials
All data generated or analyzed during this study are included in this published article.
Funding
The presented study was supported by grants from the Swiss Academy of Engineering Sciences (2014080), the 3R Research Foundation (14014), and the Swiss National Science Foundation through NCCR Kidney.CH.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Authors’ Affiliations
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