How About Glymphatic System Function in Patients With Migraine?

doi:10.21203/rs.3.rs-1041428/v1

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Research Article

How About Glymphatic System Function in Patients With Migraine?

https://doi.org/10.21203/rs.3.rs-1041428/v1

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posted 09 Nov, 2021

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Background: There have been no studies evaluating the glymphatic system function in patients with migraine. In this study, we evaluated the alterations in glymphatic system function in patients with migraine compared to healthy controls using a diffusion tensor imaging (DTI) analysis along the perivascular space (DTI-ALPS) method. We also investigated the differences in glymphatic system function between migraine patients with and without aura using the ALPS method.

Methods: We prospectively enrolled patients with migraine and healthy controls. All brain magnetic resonance imaging (MRI), including DTI, in participants, patients with migraine, and healthy controls were obtained using the same MRI scanner. We calculated the ALPS index and compared the differences in the ALPS index between patients with migraine and healthy controls, and between migraine patients with and without aura. In addition, we conducted a correlation analysis between glymphatic system function and the clinical characteristics of migraine.

Results: We enrolled 92 patients with migraine and 80 healthy controls. There were no significant differences in the ALPS index between patients with migraine and healthy controls (1.655 vs. 1.713, p = 0.233), and between migraine patients with and without aura (1.690 vs. 1.645, p = 0.601). There were no significant correlations between the ALPS index and clinical characteristics of migraine, including age (r = -0.070, p = 0.507), age of onset (r = 0.066, p = 0.552), disease duration (r = -0.115, p = 0.306), attack frequency (r = -0.049, p = 0.668), and headache intensity (r = -0.003, p = 0.976).

Conclusions: There was no glymphatic system dysfunction in patients with migraine. In addition, there were no differences in glymphatic system function between migraine patients with and without aura. We also demonstrated the feasibility of the ALPS method, which can be used for further research on various neurological diseases.

Neurology

migraine

glymphatic system

diffusion tensor imaging

Migraine is one of the most common neurological disorders, affecting approximately 12–15% of the general population.[1, 2] Migraine is more frequent in women than in men.[3] Although migraine is not a fatal disease, it is an important cause of disability worldwide and has emerged as a major global public health concern.[4]

The conceptualization and discovery of the glymphatic system has received considerable attention in the neuroscience field. It is a system that discharges interstitial waste products out of the brain, and is related to the movement of the cerebrospinal fluid (CSF) transport system.[5, 6]

Since the discovery of the glymphatic system, several methods have been proposed to evaluate glymphatic system function, and most previous studies have examined it using two-photon laser scanning microscopy.[7–10] However, this method is invasive and not a suitable tool for whole brain studies. Recently, several methods with magnetic resonance imaging (MRI) have provided non-invasive and whole brain dynamic real-time imaging for the study of glymphatic system function.[7–12] Attempts have also been made to evaluate glymphatic system function using diffusion tensor imaging (DTI), which uses the movement of water molecules in the tissue. Taoka et al. have recently proposed a DTI analysis along the perivascular space (DTI-ALPS) method based on DTI.[13] This method is to analyze the glymphatic system function by DTI under assumption that the water diffusion capacity is limited to the running direction of the perivascular space. In the DTI-ALPS method, the glymphatic system function is represented with the measures, termed ALPS index.[13]

In this study, we evaluated the alterations in glymphatic system function in patients with migraine compared to healthy controls using the ALPS method. We hypothesized that there would be glymphatic system dysfunction in patients with migraine for several reasons. First, a previous study using in vivo two-photon imaging showed that cortical spreading depression (CSD), a known instigator of migraine, produces alterations in both the structure and function of the glymphatic system.[14] CSD evokes rapid closure of the perivascular space around both arteries and veins on the pial surface of the cerebral cortex, and this closure is accompanied by a reduction in the outflow of interstitial fluid from the parenchyma into the perivascular space.[14] Second, CSD is associated with swelling of astrocytic endfeet around penetrating arterioles in the cortex of living mice, which underline closure of perivascular space and impairment of glymphatic flow.[15] Third, patients with migraine have consistently reported poor sleep quality both precipitating and during attacks. They complained of increased insomnia, including difficulty initiating sleep, staying asleep, poor sleep quality, self-reported decreased total sleep time, excessive daytime sleepiness, and lack of refreshment after sleep.[16, 17] Glymphatic system function is highly activated during sleep stage N, and CSF tracer influx correlates with the prevalence of electroencephalography slow wave activities.[6] However, there have been no studies evaluating the glymphatic system function in patients with migraine. We also investigated the differences in glymphatic system function between migraine patients with and without aura using the ALPS method. In addition, we conducted correlation analyses between glymphatic system function and the clinical characteristics of migraine.

2.1. Participants

This study was approved by the Institutional Review Board of Haeundae Paik Hospital and had a cross-sectional design. We prospectively enrolled patients with migraine at our hospital based on the following criteria: 1) visit to the neurology department from August 2018 to September 2021; 2) newly diagnosed with episodic migraine at our hospital based on the International Classification of Headache Disorders, 3rd edition,[18] who had a drug-naïve state for migraine medications; 3) normal brain MRI on fluid-attenuated inversion recovery (FLAIR) imaging and T2-weighted imaging based on visual inspection, and 4) no history of any other medical, neurological, or psychiatric disease. Written informed consent was obtained from all the participants. We investigated the demographic and clinical characteristics of patients with migraine, such as age, sex, age of onset, disease duration (the time from age of headache onset to when MRI was taken), attack frequency, and headache intensity.

We also included age- and sex-matched healthy controls who had no previous medical history, including neurological or psychiatric diseases. They had normal brain MRI on FLAIR imaging and T2-weighted imaging based on visual inspection.

2.2. MRI acquisition

All MRIs of the migraine patients and healthy controls were performed during the daytime using the same MRI scanner, which was a 3 tesla scanner with a 32-channel head coil (AchievaTx, Phillips Healthcare). They underwent the same brain MRI protocol, which included three-dimensional (3D) FLAIR imaging, coronal T2-weighted imaging, 3D T1-weighted imaging, and DTI. FLAIR and T2-weighted imaging were used to evaluate the structural abnormalities in the brain. All patients were in the interictal state of headache at the time of MRI scans (there were no migraine attacks during the MRI scanning time).

DTI was conducted using spin-echo single-shot echo-planar pulse sequences with a total of 32 different diffusion directions (TR/TE = 8620/85 ms, FA = 90^°, slice thickness = 2.25 mm, acquisition matrix = 120 × 120, field of view = 240 × 240 mm², and b-value = 1000 s/mm²).

2.3. ALPS index calculation

The method for obtaining the ALPS index was described in our previous study (Figure 1).[19, 13] Briefly, we processed the DTI data with DSI studio, such as setting up a mask, reconstruction with DTI method, and fiber tracking. Then, we drew a region of interest (ROI) in a rectangular shape and obtained the fiber orientation and diffusivities of the three directions along the x-, y-, and z-axes as voxel levels at the ROI. Finally, the DTI-ALPS index was calculated using the following formula:[13, 20]

Dxxproj: diffusivity along the x-axis in the projection fiber, Dxxassoci: diffusivity along the x-axis in the association fiber, Dyyproj: diffusivity along the y-axis in the projection fiber, Dzzassoci: diffusivity along the z-axis in the association fiber.

2.4. Statistical analysis

The primary analysis of these data was done using a priori testing. No statistical power calculations were performed prior to the study. The sample size was based on the available data. Differences in demographic and clinical characteristics between groups were analyzed using independent samples t-test or Mann–Whitney test according to normal distribution for continuous variables, and the chi-squared test was used for categorical variables. Comparisons of the ALPS index between the groups were performed using an independent samples t-test. Correlation analysis was performed using Pearson’s correlation coefficient. Categorical variables are presented as frequencies and percentages, whereas continuous variables are presented as mean ± standard deviation or median and interquartile range. Statistical significance was set at a two-tailed p < 0.05. Multiple corrections were applied when we conducted statistical analysis for diffusivities along the axis in the fibers [Bonferroni correction, p = 0.0055 (0.05/9)]. MedCalc® Statistical Software version 20.014 (MedCalc Software Ltd, Ostend, Belgium; https://www.medcalc.org; 2021) was used for the statistical analysis.

3.1. Participants

One hundred patients with newly diagnosed migraine underwent brain MRI scanning. We excluded patients with structural brain lesions or poor DTI quality (Figure 2). Finally, we included 92 patients with migraine. Eighty healthy controls were also enrolled. Table 1 shows the demographic and clinical characteristics of the migraine patients and healthy controls. Of the 92 migraine patients, 20 had migraine with aura, whereas 72 had migraine without aura. All auras experienced by migraine patients were visual aura. Age, age at onset, disease duration, and attack frequency were not different between migraine patients with and without aura. However, sex and headache intensity differed between the groups.

Table 1

Demographic and clinical characteristics in migraine patients and healthy controls
	Patients with migraine (N = 92)	Healthy controls (N = 80)	p-value
Age, years (± SD)	37.8 (± 11.7)	38.9 (± 15.2)	0.595
Male, n (%)	20 (21.7)	15 (18.7)	0.628
Age of onset, years (± SD)	28.0 (± 11.3)
Disease duration, months (interquartile range)	72 (36-204)
Attack frequency per month, n (interquartile range)	3 (2-8)
Headache intensity, visual analog scale (interquartile range)	7 (6-8)
	Migraine patients with aura (N = 20)	Migraine patients without aura (N = 72)	p-value
Age, years (± SD)	36.0 (± 12.9)	38.4 (± 11.3)	0.420
Male, n (%)	9 (45.0)	11 (15.2)	0.004
Age of onset, years (± SD)	27.7 (± 12.1)	28.6 (± 11.1)	0.740
Disease duration, months (interquartile range)	60 (12-90)	120 (36-126)	0.055
Attack frequency per month, n (interquartile range)	2 (1-8)	4 (2-8)	0.073
Headache intensity, visual analog scale (interquartile range)	6 (5-8)	7.5 (6-8)	0.020

3.2. ALPS index

There were no significant differences in the ALPS index between patients with migraine and healthy controls (1.655 vs. 1.713, p = 0.233) (Figure 3). The diffusivities along the x-axis, y-axis, and z-axis in the fibers were not different between the groups (Projection fiber; 0.58 × 10⁻³ vs. 0.59 × 10⁻³, p = 0.222; 0.40 × 10⁻³ vs. 0.39 × 10⁻³, p = 0.579; 1.02 × 10⁻³ vs. 1.05 × 10⁻³, p = 0.104; respectively) (Association fiber; 0.61 × 10⁻³ vs. 0.62 × 10⁻³, p = 0.680; 1.12 × 10⁻³ vs. 1.14 × 10⁻³, p = 0.346; 0.33 × 10⁻³ vs. 0.32 × 10⁻³, p = 0.532; respectively) (Subcortical fiber; 1.08 × 10⁻³ vs. 1.09 × 10⁻³, p = 0.479; 0.63 × 10⁻³ vs. 0.64 × 10⁻³, p = 0.796; 0.60 × 10⁻³ vs. 0.63 × 10⁻³, p = 0.241; respectively).

In addition, there were no significant differences in the ALPS index between migraine patients with and without aura (1.690 vs. 1.645, p = 0.601) (Figure 3). The diffusivities along the x-axis, y-axis, and z-axis in the fibers were not different between the groups (Projection fiber; 0.57 × 10⁻³ vs. 0.58 × 10⁻³, p = 0.566; 0.41 × 10⁻³ vs. 0.40 × 10⁻³, p = 0.896; 1.02 × 10⁻³ vs. 1.05 × 10⁻³, p = 0.973; respectively) (Association fiber; 0.59 × 10⁻³ vs. 0.62 × 10⁻³, p = 0.280; 1.10 × 10⁻³ vs. 1.13 × 10⁻³, p = 0.501; 0.30 × 10⁻³ vs. 0.34 × 10⁻³, p = 0.126; respectively) (Subcortical fiber; 1.07 × 10⁻³ vs. 1.08 × 10⁻³, p = 0.760; 0.59 × 10⁻³ vs. 0.64 × 10⁻³, p = 0.196; 0.56 × 10⁻³ vs. 0.61 × 10⁻³, p = 0.199; respectively).

3.3. Correlation analysis

There were no significant correlations between the ALPS index and clinical characteristics in migraine patients, including age (r = -0.070, p = 0.507), age of onset (r = 0.066, p = 0.552), disease duration (r = -0.115, p = 0.306), attack frequency (r = -0.049, p = 0.668), and headache intensity (r = -0.003, p = 0.976).

The main findings of this study were as follows: 1) there was no glymphatic system dysfunction in patients with migraine compared to healthy controls, 2) no differences in glymphatic system function were found between migraine patients with and without aura, 3) there were no significant correlations between the clinical characteristics of migraine and glymphatic system function, and 4) we demonstrated the feasibility of the ALPS method for research in neurological disorders.

Recently, several studies have utilized the ALPS method to evaluate glymphatic system function in various neurological diseases, such as Alzheimer’s disease,[13] normal pressure hydrocephalus,[21] Parkinson’s disease,[22] cerebral small vessel disease,[23] and juvenile myoclonic epilepsy.[19] They successfully demonstrated glymphatic system dysfunction in neurological diseases. In addition, these studies found a significant positive correlation between the ALPS index and cognitive function, and a negative correlation between the ALPS index and age. Our study, along with the previous studies, also proved the usefulness of the ALPS method to assess glymphatic system function, and it is expected that it can be used to investigate glymphatic system function in various neurological diseases in the future. This ALPS method has the advantages of being non-invasive and not requiring gadolinium-based contrast agents.

However, contrary to our initial hypothesis, we found no alterations in glymphatic system function in patients with migraine compared to healthy controls. Although the exact causes are unknown, several possibilities can be considered. First, migraine is not a neurodegenerative disease. Glymphatic system dysfunction is implicated in a variety of neurologic diseases, particularly in neurodegenerative diseases, including dementia, Parkinson’s disease, and normal pressure hydrocephalus.[24] There is little evidence showing that patients with migraine can be prone to any neurodegenerative diseases.[25–27] A previous study prospectively assessed the association between migraine and dementia, and found no association between them.[25] Another study that evaluated whether there was any correlation between headache and Parkinson’s disease revealed no such association.[27] In addition, there is an age-associated decline in glymphatic system function, and this appears to be related to reduced penetrating arterial pulsatility in the aged brain.[28, 24] Prevalence of migraine peaks between the ages of 30 and 39, and falls to reach the lowest prevalence in those 60 and older.[29] Furthermore, there were no significant correlations between the clinical characteristics of migraine and glymphatic system function in our study, which also represented glymphatic system dysfunction actually being absent in patients with migraine. Second, all MRI scans of patients with migraine were performed during the interictal period, and not during migraine attacks, to increase the homogeneity of imaging. The possibility that glymphatic system function differs depending on the presence or absence of a headache attack cannot be excluded. Third, MRI scans were performed during daytime in all participants. Since the glymphatic system function is activated especially during deep sleep stage N, the glymphatic system function between patients with migraine and healthy controls can be different during sleep. To confirm these assumptions, DTI scanning is required during the ictal period and during sleep.

We also found no differences in glymphatic system function between patients with migraine with and without aura. Recently, it was demonstrated that CSD, the neural event that underlies migraine aura, results in the temporary impairment of glymphatic flow in a mouse model via closure of the paravascular spaces for several minutes after the induction of CSD, followed by a gradual recovery over half an hour.[14] Additionally, we recently demonstrated that there were considerable differences in the brain network between migraine patients with and without aura.[30] Thus, we initially thought that there would be differences in glymphatic system function depending on the presence or absence of aura. The present negative results in this study might have originated from the small number of migraine patients with aura, or owing to problems with MRI scanning time, as already mentioned above.

This was the first study to evaluate glymphatic system function in patients with migraine. We enrolled a large number of patients with migraine and healthy controls. However, this study has several limitations. First, we excluded patients with structural brain lesions on MRI. However, migraine is commonly associated with white matter hyperintensities.[31] Although the ALPS index is a ratio of diffusivities and the influence of white matter hyperintensities might be mitigated by this division calculation, white matter hyperintensities would influence the ALPS index. Second, the ALPS index can be affected by several factors, including imaging plane, head position, and motion-proving gradients.[20] However, a previous report showed that the results of the ALPS method were significantly related to glymphatic system function calculated by intrathecal administration of gadolinium-based contrast agent on MRI,[23] and another study successfully demonstrated good test-retest reproducibility and robustness of the ALPS method.[20]

There is no glymphatic system dysfunction in patients with migraine. In addition, there were no differences in glymphatic system function between patients with migraine with and without aura. We also demonstrated the feasibility of the ALPS method, which can be used for further research on various neurological diseases.

Ethics approval and consent to participate

This study was approved by the Institutional Review Board of Haeundae Paik Hospital and had a cross-sectional design. Written informed consent was obtained from all participants.

Consent for publication

Not applicable.

Availability of data and materials

The datasets supporting the conclusions of this article are included within the article and its additional files.

Competing interests

The authors declare that they have no competing interests.

Funding

None.

Authors' contributions

DA Lee, BS Lee and KM Park conceived and designed the analysis, analyzed and interpreted the data, drafted and revised the manuscript for intellectual content. J Ko, IH Kim, JH Park, S Park, EJ Lee and KM Park performed data acquisition, analyzed and interpreted the data, revised the manuscript for intellectual content. All authors read and approved the final manuscript.

Acknowledgements

None.

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How About Glymphatic System Function in Patients With Migraine?

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Abstract

Figures

1. Background

2. Methods

2.1. Participants

2.2. MRI acquisition

2.3. ALPS index calculation

2.4. Statistical analysis

3. Results

3.1. Participants

3.2. ALPS index

3.3. Correlation analysis

4. Discussion

5. Conclusion

Declarations

References

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