Prognostic value of the preoperative study of cerebrospinal fluid dynamics in Chiari malformations: a pilot study

doi:10.21203/rs.3.rs-6951398/v1

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Research Article

Prognostic value of the preoperative study of cerebrospinal fluid dynamics in Chiari malformations: a pilot study

https://doi.org/10.21203/rs.3.rs-6951398/v1

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Journal Publication

published 21 Nov, 2025

Read the published version in Acta Neurochirurgica →

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Purpose

In patient with Chiari type I malformations (CMI), indication for surgery can be difficult to establish. Headaches are a common complaint. Factors that predict headache relief have not been clearly identified. Various research has attempted to understand the hydrodynamic in patient with CMI by applying phase-contrast MRI (pcMRI) – only non-invasive technique for studying craniospinal hydrodynamics and hemodynamic. People with CMI present alterations in cerebrospinal fluid (CSF) and cerebral blood dynamics. The objective of the present study was to identify hydrodynamic criteria that are predictive of positive clinical outcome (headache relief) after posterior fossa decompression surgery in patient with CMI.

Method

41 patients who underwent posterior fossa decompression surgery at Amiens-Picardie University Hospital (Amiens, France) between 2016 and 2021 were retrospectively included. We used preoperative pcMRI to analyze CSF dynamics. CSF stoke volume were measured at the level of aqueduct of Sylvius (SV_aqu), subarachnoid spaces near to C2-C3 (SV_C2C3) vertebral junction, prepontine cisterns, foramen magnum, and brainstem. CSF pulsatility was studied as a function of the postoperative headache relief reported (or not) by patients. Statistical analyses were based on Student's t-test.

Results

12 patients reported headache relief. The mean SV_aqu was significantly higher in patients with headache relief than in those without relief (65 and 32.13µL/CC, p ≤ 0.05). The mean SV_C2−C3 was significantly lower in patients with headache relief than in patients without relief (484.58 and 612.94µL/CC, p ≤ 0.05). The two groups of patients did not differ significantly in terms of the area of the narrowest part of the aqueduct of Sylvius or the Evans index.

Conclusion

SVaqu might have prognostic value for headache relief after CMI surgery. Further analysis is needed. This is probably related to recruitment of intraventricular pulsatility, which helping regulate potential intracranial pressure alteration. This pulsatility doesn't seem related to morphology.

phase-contrast MRI

Chiari malformation

cerebrospinal fluid dynamics

Chiari malformation type I (CMI) is defined radiologically by ptosis of the cerebellar tonsils of more than 5 mm below the McRae line¹. The latter connects the inferior edge of the clivus to the occipital border and defines the plane of the foramen magnum. The signs and symptoms associated with CMI are not specific. Some patients report Otorhinolaryngologic disorders, spinal cord involvement, bulbar involvement, or visual disturbances². The most commonly reported symptom by patients is headache³ described conventionally as pulsatile, accentuated by effort and by coughing, with radiation to the vertex. CMI-related headache has a major impact on the patient’s quality of life and is often resistant to drug treatment³. Some patients report so-called atypical headaches that are also refractory to drug treatment and are not always linked to differential diagnoses of CMI⁴.

When symptoms significantly impair the patient’s quality of life, surgical treatment may be considered. The standard procedure involves posterior fossa decompression, with or without duroplasty⁵. The type of surgery does not appear to predict the clinical outcome but posterior fossa decompression with duraplasty seems to be more effective on clinical outcome^6,7. The key issue for surgery in CMI is the selection of patients whose symptoms are likely to be relieved by surgery⁸. It should be borne in mind that this surgical treatment is associated with significant morbidity; according to the literature data, the overall postoperative complication rate is 21.8%, with neurological deterioration in 14.3% of cases⁹. Furthermore, 21% of patients reported no symptom relief (including headache) after surgery⁹. Establishing the indication for surgery can be challenging due to the current lack of clearly identified predictive factors for postoperative relief of headache associated with CMI. Only occipital throbbing headaches that radiate towards the vertex exhibit favorable outcomes following surgical treatment⁴. Other types of headaches have an uncertain prognosis for improvement. These studies provide a set of arguments to guide the choice of management but do not provide a formal prediction of treatment effectiveness.

The etiology of CMI remains unclear¹⁰. Some studies have shown that the patient’s symptoms are not related to the degree of ptosis of the cerebellar tonsils¹¹. The clinical outcome does not appear to be directly related to morphological variables¹². We therefore decided to study the cerebrospinal fluid (CSF) hydrodynamics, with a view to better understanding the genesis of CMI entity and its symptoms^13,14. During systole, a sharp increase in cerebral arterial blood flow leading to a sudden inflow of arterial blood into the cranium^17,18. This inflow is fully compensated for by an outflow of venous blood^15,16. However, arterial and venous flows are not synchronized throughout the cardiac cycle (CC), resulting in an increase in intracranial vascular volume during systole. In healthy individuals, subarachnoid CSF is rapidly flushed into the perimedullary subarachnoid spaces during systole and thus compensates almost instantaneously for variations in intracranial vascular volume^15,16 (Fig. 1). The pulsatility of subarachnoid contribute to overall intracranial compliance. Hence, CSF oscillations in the foramen magnum over the CC have a major role in the regulation of intracranial pressure.

Patients with CMI show alterations in CSF and blood dynamics^17–22. The ptosis of the cerebellar tonsils reduces the area of the subarachnoid spaces at the level of foramen magnum, thus increasing the resistance to CSF flow. In a number of cases, pulsatility is transmitted to the cerebellar tonsils and neuraxis and might be a clear marker of CMI^17,18,22. These hydrodynamic changes may be linked to specific CMI symptoms. Phase-contrast MRI (pcMRI) is the only non-invasive method for analyzing CSF and blood dynamics during the CC.

This preliminary study aimed to determine whether preoperative analysis of CSF dynamics can predict postoperative headache relief in patients with CMI.

2.1 Patients

All patients with CMI having undergone bone decompression surgery in Amiens-Picardie University Hospital (Amiens, France) between 2016 and 2021 were included retrospectively in the study. All patients underwent bone posterior fossa decompression with or without duraplasty. In all cases, the diagnosis of CMI was based on morphological MRI features. The characteristics of each patient were documented at the first diagnostic consultation for CMI. Postoperative headache relief was defined as a decrease of more than two points on a pain visual analogue scale, together with and an improvement in quality of life. No other symptoms were considered in the present study. The surgical indications were based on a set of clinico-radiological arguments and not solely on headaches.

2.2 Imaging

2.2.1 MRI acquisition

Each patient was diagnosed with CMI on the basis of morphological MRI features. At the Amiens-Picardie University Hospital, each patient diagnosed with CMI is examined with additional pcMRI sequences before any surgical treatment. Brain MRI was performed on a 3 Tesla system (Philips Achieva), the parameters of which are summarized in Table 1. During pcMRI acquisition, the encoding speed was set to 10 cm/s for measurement of the stroke volume (SV) of CSF passing through the aqueduct of Sylvius and to 5 cm/s for acquisitions in other planes.

Table 1

Acquisition parameters for phase-constrast MRI.
	pcMRI
Field of view (cm²)	14x14 or 16x16
Resolution (mm²)	0.6x0.6
Slice thickness (mm²)	2
Flip angle (degrees)	30
Sensitivity encoding	1.5
Echo time (ms)	Minimum
Repetition time (ms)	Minimum
Number of images	32
Acquisition time (s)	50–115
Number of images per cycle	32

The pcMRI measurements were synchronized with the patient's heart rate by using retrospective plethysmographic gating; this enabled us to measure the change in velocity over 32 time points in the CC. The pcMRI images were analyzed using Flow® software (version 2.0, 2018) developed in-house at Amiens-Picardie University Hospital.

2.2.2 pcMRI post-processing

Using the preoperative pcMRI data, we reconstructed a voxel-by-voxel CSF velocity curve. For each predefined slice plane, the area of interest was semi-automatically segmented using Flow® software (Fig. 2). Each voxel in the area of interest corresponded to a CSF velocity during a CC. The resulting curve indicated the flow of CSF through the area of interest (Fig. 2). This flow curve was then integrated to obtain the SV of CSF passing through the area of interest during a CC (Fig. 2). By repeating this method for each plane and each area of interest, we calculated the CSF SVs at several precise anatomical areas of interest over the course of a CC¹⁷: the mesencephalic aqueduct (SVaqu), the cervical subarachnoid spaces near the C2-C3 vertebral junction (SVc2c3), the prepontine cisterns (SVppc), and the foramen magnum (SVfm), and the cerebellar tonsils near the foramen magnum (SVtonsils) (Fig. 3).

2.2.2 Measurement of the area of the aqueduct of Sylvius

The area (mm²) of the aqueduct of Sylvius was measured on axial slices of 3D T2 fast field echo acquisitions before surgery. The latter sequence provides better contrast between tissue and fluid signals. On sagittal slices, the slice where the aqueduct of Sylvius is narrowest was reconstructed as an axial section. The region of interest was then selected manually.

2.2.3 Measurement of the Evans index

For each patient, the Evans index was determined from preoperative morphological MRI data (axial sections from fluid-attenuated inversion recovery sequences). The Evans index is defined as the ratio between the maximum width of the frontal horns and the maximum biparietal cranium diameter and is a marker of ventriculomegaly²³. All measurements of the Evans index were performed manually by the same person.

2.2 Statistics

Statistical analyses were based on Student's t-test. The normality of the data distribution was checked with the Kolmogorov-Smirnov test. The threshold for statistical significance was set to p≤0.05. A non-parametric Mann-Whitney test was applied to the intergroup comparison of the area of the aqueduct of Sylvius and the Evans indexes because the data for these variables were not normally distributed.

2.3 Ethics

The study protocol was approved by the local institutional review board (CPP Nord Ouest II, Amiens, France; reference: HYDROAQU-C PI2024_843_0028). In line with the French legislation on retrospective observational studies of clinical practice, patient consent was not required.

Clinical data

A total of 41 patients (37 women and 4 men) were included (Table 2). The mean age was 39. At the post-operative follow-up visit, 12 patients reported headache relief and 29 reported no relief). The groups with and without relief did not differ significantly with regard to demographic data or the preoperative symptom profile (Tables 2 and 3). The postoperative improvement rate (CCOS between 13 and 16) was 92.7% (38 out of 41 patients).

Table 2

Demographic characteristics of the study population, according to the presence or absence of headache relief after surgery.
Population	Headache relieved	Headache not relieved
Number of patients	12	29
Sex ratio (M/F)	3/9	3/26
Mean ± SD age (years)	45 ± 12	39 ± 11

Table 3

The prevalence of symptoms (expressed as the number of affected patients) before surgery, according to the presence or absence of headache relief after surgery.
	Headache relieved (n = 12)	Headache not relieved (n = 29)	p value
Headache	12	29	1
Torticollis	2	3	0.6
Spinal cord injuries	6	10	0.48
Sleep apnoea	4	7	0.7
Vertigo	5	4	0.09
Gait instability	4	2	0.05
Nystagmus	2	2	0.57
Visual blurring	1	2	1
Tinnitus	0	1	1
Vestibular disorders	1	1	0.5
Swallowing disorders	4	4	0.2
Breathlessness	0	2	1
Hydrocephalus	3	1	0.07
Syringomyelia	6	8	0.28

Hydrodynamic parameters

On preoperative pcMRI, the mean SV_aqu was significantly higher in patients with headache relief than in those without relief (65 and 32.13 µL per CC, respectively; p ≤ 0.05) (Table 4), and the mean SV_C2−C3 was significantly lower in patients with headache relief than in patients without relief after surgery (484.58 and 612.94 µL per CC, respectively; p ≤ 0.05).

Table 4

The preoperative mean ± SD CSF SVs over the course of a CC in patients with vs. without headache relief. * Indicates a statistically significant difference (p ≤ 0.05) in Student's t-test after the normality of the data distribution had been confirmed in the Kolmogorov Smirnov test.
SV (µL per CC)	Headache relieved (n = 12)	Headache not relieved (n = 29)	p
SV_aqu	65 ± 45.48	32.13 ± 24.22	0.03*
SV_ppc	334.27 ± 262.4	410 ± 171.88	0.32
SV_fm	435.83 ± 301.37	504.07 ± 225.17	0.62
SV_nevrax	248 ± 155.1	156.94 ± 108.74	0.19
SV_C2−C3	484.58 ± 162.69	612.94 ± 165.66	0.03*

Although the postoperative ranges of CSF SV values in the two patient groups overlapped, an SV_aqu value greater than 100 µL per CC was only observed in patients with headache relief after surgery, and a value below 18µL per CC was only observed in patients without headache relief after surgery (Fig. 4). An SVC2-C3 value below 300 µL per CC was only observed in the patients with headache relief, and a value above 800 µL per CC was only observed in patients without headache relief.

Table 5

Mean ± SD area of the narrowest part of the aqueduct of Sylvius areas opposite the smallest section, measured on axial-section 3D fast field echo MRI, and the mean ± SD Evans index measured on axial-section fluid-attenuated inversion recovery MRI.
	Headache relieved (n = 12)	Headache not relieved (n = 29)	P
Aqueduct area (mm²)	6.47 ± 2.05	5.76 ± 1.86	0.22
Evans’ index	0.29 ± 0.07	0.24 ± 0.04	0.06

Morphological data

The two groups of patients did not differ significantly in terms of the area of the narrowest part of the aqueduct of Sylvius or the Evans index (Table 5).

Our present results highlight the value of pcMRI for the preoperative evaluation of CMI. Indeed, high preoperative intraventricular CSF pulsatility has prognostic value with regard to postoperative headache relief. This finding might help physicians to select patients for surgery or, in contrast, to recommend drug treatment alone, with a view to avoiding potential post-operative morbidity in the absence of likely clinical benefits.

Headaches

According to some research, the typically pulsatile CMI-associated headaches appear to respond better to surgery than atypical headaches do⁴. Our study included both patients with typical headaches (pulsatile, accentuated by effort and by coughing, with radiation to the vertex) and patients with atypical headaches (all other types). However, some patients with atypical headaches experience clinical relief after surgery, and so it is difficult to base selection for surgery purely on the patient’s subjective description of headache; objective variables (such as those based on pcMRI data) are needed. The preoperative profile of symptoms other than headache did not appear to have prognostic value because it was similar in patients with vs. without postoperative headache relief.

Hydrodynamics and prognostic assessment

A few research have studied the relationship between craniospinal hydrdynamics and symptoms. Several studies have shown the link between the presence of symptoms and MICs, without reaching the point of being a definitive marker^19,24.

However, these studies focused solely on the maximum flow velocity of the CSF or blood. The volume displaced depends directly in the pressure gradient²⁵. Hence, an analysis of the displaced volume appears to be entirely appropriate. Some research have already described the value of pcMRI for predicting postoperative clinical improvement in patients with CMI^19–21,24. McGirt et al.²⁴ demonstrated that normal preoperative CSF flow in the hindbrain, assessed by pcMRI, was an independent risk factor for failure to achieve postoperative headache relief in patients with CMI. PcMRI may prove useful in selecting Chiari I malformation patients who are at higher risk of poor response to surgical decompression.²⁴ A high preoperative SVaqu appears to predict postoperative headache relief. This might be due to the recruitment of ventricular compliance during CMI subarachnoid compliance might change as a result of ptosis of the cerebellar tonsils, with greater flow resistance in this area.

Our present results also indicate that changes in the dynamics of the cervical subarachnoid CSF might be related to the postoperative prognosis for headaches. According to other studies, a decrease in postoperative CSF dynamics (a decrease of at least 20% in SVc2c3, specifically) is associated with headache relief²¹. Nevertheless, this significant difference appears to have less clinical relevance than an analysis of intraventricular CSF dynamics. Indeed, an analysis of the distribution of CSF hydrodynamic profiles (Fig. 4) shows that most of patients presented similar profiles. This similarity might be linked to different hemodynamic profiles. Indeed, CSF pulsatility is directly related to variations in intracranial vascular volume¹⁶.

Aqueduct area and Evans index

According to Poiseuille's law, fluid flow depends on the pressure gradient, flow area, and fluid viscosity. Intraventricular CSF dynamics result from variations in the pressure gradient between the 3rd and 4th ventricles. The viscosity of CSF does not change. There was no significant difference in the cross-sectional area of the midbrain aqueduct between patients with headache relief and those without. The increase in intraventricular CSF dynamics therefore appears to be related to variations in the pressure gradient between the 3rd and 4th ventricles. It would therefore be interesting to measure the pressure gradient on either side of the aqueduct of Sylvius, in order to determine whether or not this variable is related to clinical relief of headache after surgery. This gradient might be responsible for high intraventricular pulsatility.

The results of several studies of patients with normal pressure hydrocephalus have demonstrated that the SV at the aqueduct of Sylvius depends essentially on the ventricular volume²⁶. In our study, we observed a higher preoperative CSF SV in the group of patients with headache relief. However, this SV was not linked to an increase in ventricular volume because the two groups of patients did not differ significantly with regard to the Evans index - a good marker of ventriculomegaly. Furthermore, recent studies suggest that combining preoperative assessments of cerebrospinal fluid hydrodynamics with morphological analysis of the fourth ventricle outlet improves the predictive accuracy of postoperative clinical outcomes in patients undergoing decompression surgery CMI²⁷. An increase in ventricular pulsatility (highlighted in our study by the increase in the SV of the aqueduct of Sylvius) in patients with postoperative improvement does not therefore appears to be linked to an increase in ventricular volume: whatever the preoperative ventricular volume, the ventricular pulsatility increases. Pulsatility does not therefore appear to be linked to ventricular volume.

Study limitations

Firstly, our study included a small number of patients; further studies of larger populations are needed to confirm the present results. Secondly, our study was retrospective study, and so further prospective studies are required including headache-specific score assessment. Thirdly, our analyses were limited to CSF dynamics, which are secondary to variations in intracranial arteriovenous volume. Hence, studies focusing on arteriovenous variables might provide further prognostic evidence of postoperative clinical improvements in patients. Future studies could assess both variations in CSF volumes and changes in arterial and venous volume dynamics during the CC. Breathing also influences hemodynamics during the CC. It would be interesting to study of respiratory variations during the CC in this context.

Preoperative high intraventricular CSF dynamics might to be related to headache relief after posterior fossa decompression surgery in patients with CMI. This alteration in CSF dynamics might be linked to changes during the CC.

Ethical Approval, consent to participate, consent to publish :

Not applicable

Competing interests :

No competing interests

Funding :

Not applicable

Author Contribution

P.C collected the data, carried out the statistical tests and wrote the article and figures.C.C directed the study, checked the validity of the data, reviewed the manuscript and made the necessary corrections.O.B co-led the study, interpreted the imaging studies and made the data available for collection.J.P reviewed the manuscript.R.L helped with data collection.

Availability of data and materials :

The data is stored at the university hospital in the patient file, and has been collected and stored in an excel file also kept at the university hospital.

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No competing interests reported.

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You are reading this latest preprint version

Prognostic value of the preoperative study of cerebrospinal fluid dynamics in Chiari malformations: a pilot study

Status:

Journal Publication

Version 1

Abstract

Purpose

Method

Results

Conclusion

Figures

1 Introduction

2 Material and methods

2.1 Patients

2.2 Imaging

2.2.1 MRI acquisition

2.2.2 pcMRI post-processing

2.2.2 Measurement of the area of the aqueduct of Sylvius

2.2.3 Measurement of the Evans index

2.2 Statistics

2.3 Ethics

3 Results

4 Discussion

5 Conclusion

Declarations

Ethical Approval, consent to participate, consent to publish :

Competing interests :

Funding :

Author Contribution

Availability of data and materials :

References

Additional Declarations

Status:

Journal Publication

Version 1