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Detection of changes in the periaqueductal gray matter of patients with episodic migraine using quantitative diffusion kurtosis imaging: preliminary findings

  • Diagnostic Neuroradiology
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Abstract

Introduction

The periaqueductal gray matter (PAG) is considered to play an important role in generating migraine, but findings from imaging studies remain unclear. Therefore, we investigated whether diffusion kurtosis imaging (DKI) can detect changes in the PAG of migraine patients.

Methods

We obtained source images for DKI from 20 patients with episodic migraine and 20 healthy controls using a 3 T magnetic resonance imaging scanner. Mean kurtosis (MK), fractional anisotropy (FA), and mean diffusivity (MD) maps were generated, and the values of the PAG and other deep gray and white matter structures were automatically measured using an atlas-based region-of-interest analysis. The metrics of these structures were compared between the patients and controls.

Results

The MK and MD values of the PAG were significantly increased in the migraine patients compared with the controls (p < 0.05). The FA values were not significantly different. There were no significant differences in the metrics of the other structures between the patients and controls. The MK values of the PAG were significantly positively correlated with both age and the untreated period in the patient group under univariate analysis (r = 0.53 and 0.56, respectively; p < 0.05) but not multivariate analysis.

Conclusions

DKI detected significant increases in the MK and MD values of the PAG in patients with migraine, which suggests that structural changes in the PAG are associated with the pathophysiological mechanisms of migraine.

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References

  1. Tfelt-Hansen PC, Koehler PJ (2011) One hundred years of migraine research: major clinical and scientific observations from 1910 to 2010. Headache 51:752–778. doi:10.1111/j.1526-4610.2011.01892.x

    Article  PubMed  Google Scholar 

  2. Hoskin KL, Bulmer DC, Lasalandra M, Jonkman A, Goadsby PJ (2001) Fos expression in the midbrain periaqueductal grey after trigeminovascular stimulation. J Anat 198:29–35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Weiller C, May A, Limmroth V, Juptner M, Kaube H, Schayck RV, Coenen HH, Diener HC (1995) Brain stem activation in spontaneous human migraine attacks. Nat Med 1:658–660

    Article  CAS  PubMed  Google Scholar 

  4. Welch KM, Nagesh V, Aurora SK, Gelman N (2001) Periaqueductal gray matter dysfunction in migraine: cause or the burden of illness? Headache 41:629–637

    Article  CAS  PubMed  Google Scholar 

  5. Rocca MA, Ceccarelli A, Falini A, Colombo B, Tortorella P, Bernasconi L, Comi G, Scotti G, Ref Filippi M (2006) Brain gray matter changes in migraine patients with T2-visible lesions: a 3-T MRI study. Stroke 37:1765–1770. doi:10.1161/01.STR.0000226589.00599.4d

    Article  PubMed  Google Scholar 

  6. Hosobuchi Y, Adams JE, Linchitz R (1977) Pain relief by electrical stimulation of the central gray matter in humans and its reversal by naloxone. Science 197:183–186

    Article  CAS  PubMed  Google Scholar 

  7. Raskin NH, Hosobuchi Y, Lamb S (1987) Headache may arise from perturbation of brain. Headache 27:416–420

    Article  CAS  PubMed  Google Scholar 

  8. Kruit MC, Launer LJ, Overbosch J, van Buchem MA, Ferrari MD (2009) Iron accumulation in deep brain nuclei in migraine: a population-based magnetic resonance imaging study. Cephalalgia 29:351–359. doi:10.1111/j.1468-2982.2008.01723.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. DaSilva AF, Granziera C, Tuch DS, Snyder J, Vincent M, Hadjikhani N (2007) Interictal alterations of the trigeminal somatosensory pathway and periaqueductal gray matter in migraine. Neuroreport 18:301–305. doi:10.1097/WNR.0b013e32801776bb

    Article  PubMed  PubMed Central  Google Scholar 

  10. Neeb L, Bastian K, Villringer K, Gits HC, Israel H, Reuter U, Fiebach JB (2015) No microstructural white matter alterations in chronic and episodic migraineurs: a case-control diffusion tensor magnetic resonance imaging study. Headache 55:241–251. doi:10.1111/head.12496

    Article  PubMed  Google Scholar 

  11. Jensen JH, Helpern JA (2010) MRI quantification of non-Gaussian water diffusion by kurtosis analysis. NMR Biomed 23:698–710. doi:10.1002/nbm.1518

    Article  PubMed  PubMed Central  Google Scholar 

  12. Headache Classification Subcommittee of the International Headache S (2004) The international classification of headache disorders: 2nd edition. Cephalalgia 24(Suppl 1):9–160

    Google Scholar 

  13. Yokosawa S, Sasaki M, Bito Y, Ito K, Yamashita F, Goodwin J, Higuchi S, Kudo K (2015) Optimization of scan parameters to reduce acquisition time for diffusion kurtosis imaging at 1.5 T. Magn Reson Med Sci (in press). doi:10.2463/mrms.2014-0139

    Google Scholar 

  14. Ito K, Sasaki M, Ohtsuka C, Yokosawa S, Harada T, Uwano I, Yamashita F, Higuchi S, Terayama Y (2015) Differentiation among parkinsonisms using quantitative diffusion kurtosis imaging. Neuroreport 26:267–272. doi:10.1097/Wnr.0000000000000341

    Article  CAS  PubMed  Google Scholar 

  15. Yuan K, Qin W, Liu P, Zhao L, Yu D, Zhao L, Dong M, Liu J, Yang X, von Deneen KM, Liang F, Tian J (2012) Reduced fractional anisotropy of corpus callosum modulates inter-hemispheric resting state functional connectivity in migraine patients without aura. PLoS One 7:e45476. doi:10.1371/journal.pone.0045476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Li XL, Fang YN, Gao QC, Lin EJ, Hu SH, Ren L, Ding MH, Luo BN (2011) A diffusion tensor magnetic resonance imaging study of corpus callosum from adult patients with migraine complicated with depressive/anxious disorder. Headache 51:237–245. doi:10.1111/j.1526-4610.2010.01774.x

    Article  PubMed  Google Scholar 

  17. Yu D, Yuan K, Qin W, Zhao L, Dong M, Liu P, Yang X, Liu J, Sun J, Zhou G, von Deneen KM, Tian J (2013) Axonal loss of white matter in migraine without aura: a tract-based spatial statistics study. Cephalalgia 33:34–42. doi:10.1177/0333102412466964

    Article  PubMed  Google Scholar 

  18. DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845

    Article  CAS  PubMed  Google Scholar 

  19. Yendiki A, Koldewyn K, Kakunoori S, Kanwisher N, Fischl B (2013) Spurious group differences due to head motion in a diffusion MRI study. Neuroimage 88C:79–90. doi:10.1016/j.neuroimage.2013.11.027

    PubMed  Google Scholar 

  20. Bashir A, Lipton RB, Ashina S, Ashina M (2013) Migraine and structural changes in the brain: a systematic review and meta-analysis. Neurology 81:1260–1268. doi:10.1212/WNL.0b013e3182a6cb32

    Article  PubMed  PubMed Central  Google Scholar 

  21. Hougaard A, Amin FM, Ashina M (2014) Migraine and structural abnormalities in the brain. Curr Opin Neurol 27:309–314. doi:10.1097/WCO.0000000000000086

    Article  PubMed  Google Scholar 

  22. Szabo N, Kincses ZT, Pardutz A, Tajti J, Szok D, Tuka B, Kiraly A, Babos M, Voros E, Bomboi G, Orzi F, Vecsei L (2012) White matter microstructural alterations in migraine: a diffusion-weighted MRI study. Pain 153:651–656. doi:10.1016/j.pain.2011.11.029

    Article  PubMed  Google Scholar 

  23. Zhuo J, Xu S, Proctor JL, Mullins RJ, Simon JZ, Fiskum G, Gullapalli RP (2012) Diffusion kurtosis as an in vivo imaging marker for reactive astrogliosis in traumatic brain injury. Neuroimage 59:467–477. doi:10.1016/j.neuroimage.2011.07.050

    Article  PubMed  PubMed Central  Google Scholar 

  24. Valonen PK, Lehtimaki KK, Vaisanen TH, Kettunen MI, Grohn OH, Yla-Herttuala S, Kauppinen RA (2004) Water diffusion in a rat glioma during ganciclovir-thymidine kinase gene therapy-induced programmed cell death in vivo: correlation with cell density. J Magn Reson Imaging 19:389–396. doi:10.1002/jmri.20026

    Article  PubMed  Google Scholar 

  25. Hemanth Kumar BS, Mishra SK, Trivedi R, Singh S, Rana P, Khushu S (2014) Demyelinating evidences in CMS rat model of depression: a DTI study at 7 T. Neuroscience 275:12–21. doi:10.1016/j.neuroscience.2014.05.037

    Article  CAS  PubMed  Google Scholar 

  26. Nowrangi MA, Okonkwo O, Lyketsos C, Oishi K, Mori S, Albert M, Mielke MM (2015) Atlas-based diffusion tensor imaging correlates of executive function. J Alzheimers Dis 44:585–598. doi:10.3233/JAD-141937

    PubMed  PubMed Central  Google Scholar 

  27. Adluru N, Destiche DJ, Lu SY, Doran ST, Birdsill AC, Melah KE, Okonkwo OC, Alexander AL, Dowling NM, Johnson SC, Sager MA, Bendlin BB (2014) White matter microstructure in late middle-age: effects of apolipoprotein E4 and parental family history of Alzheimer’s disease. Neuroimage Clin 4:730–742. doi:10.1016/j.nicl.2014.04.008

    Article  PubMed  PubMed Central  Google Scholar 

  28. Stebbins GT, Murphy CM (2009) Diffusion tensor imaging in Alzheimer’s disease and mild cognitive impairment. Behav Neurol 21:39–49. doi:10.3233/BEN-2009-0234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Oishi K, Faria A, Jiang H, Li X, Akhter K, Zhang J, Hsu JT, Miller MI, van Zijl PC, Albert M, Lyketsos CG, Woods R, Toga AW, Pike GB, Rosa-Neto P, Evans A, Mazziotta J, Mori S (2009) Atlas-based whole brain white matter analysis using large deformation diffeomorphic metric mapping: application to normal elderly and Alzheimer’s disease participants. Neuroimage 46:486–499. doi:10.1016/j.neuroimage.2009.01.002

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was partially supported by a Grant-in-Aid for Strategic Medical Science Research (S1491001) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan.

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Corresponding author

Correspondence to Kenji Ito.

Ethics declarations

We declare that all human studies have been approved by the Institutional Ethics Committee and have therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. We declare that all patients gave informed consent prior to inclusion in this study.

Conflict of interest

SY is an employee of Hitachi, Ltd. MS has received an honorarium and research grant from Hitachi Medical Corp.

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Ito, K., Kudo, M., Sasaki, M. et al. Detection of changes in the periaqueductal gray matter of patients with episodic migraine using quantitative diffusion kurtosis imaging: preliminary findings. Neuroradiology 58, 115–120 (2016). https://doi.org/10.1007/s00234-015-1603-8

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  • DOI: https://doi.org/10.1007/s00234-015-1603-8

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