Structural and functional brain changes in perimenopausal women who are susceptible to migraine: a study protocol of multi-modal MRI trial

Bo Hu, Xu Wang, Jie-Bing He, Yu-Jie Dai, Jin Zhang, Ying Yu, Qian Sun, Lin-FengYan, Yu-Chuan Hu, Hai-Yan Nan, Yang Yang, Alan D Kaye, Guang-Bin Cui, Wen Wang, Bo Hu, Xu Wang, Jie-Bing He, Yu-Jie Dai, Jin Zhang, Ying Yu, Qian Sun, Lin-FengYan, Yu-Chuan Hu, Hai-Yan Nan, Yang Yang, Alan D Kaye, Guang-Bin Cui, Wen Wang

Abstract

Background: As a common clinical symptom that often bothers midlife females, migraine is closely associated with perimenopause. Previous studies suggest that one of the most prominent triggers is the sudden decline of estrogen during perimenopausal period. Hormone replacement therapy (HRT) is widely used to prevent this suffering in perimenopausal women, but effective diagnostic system is lacked for quantifying the severity of the diseaase. To avoid the abuse and overuse of HRT, we propose to conduct a diagnostic trial using multimodal MRI techniques to quantify the severity of these perimenopausal migraineurs who are susceptible to the decline of estrogen.

Methods: Perimenopausal women suffering from migraine will be recruited from the pain clinic of our hospital. Perimenopausal women not suffering from any kind of headache will be recruited from the local community. Clinical assessment and multi-modal MR imaging examination will be conducted. A follow up will be conducted once half year within 3 years. Pain behavior, neuropsychology scores, fMRI analysis combined with suitable statistical software will be used to reveal the potential association between these above traits and the susceptibility of migraine.

Discussion: Multi-modal imaging features of both healthy controls and perimenopausal women who are susceptible to estrogen decline will be acquired. Imaging features will include volumetric characteristics, white matter integrity, functional characteristics, topological properties, and perfusion properties. Clinical information, such as basic information, blood estrogen level, information of migraine, and a bunch of neurological scale will also be used for statistic assessment. This clinical trial would help to build an effective screen system for quantifying the severity of illness of those susceptible women during the perimenopausal period.

Trial registration: This study has already been registered at Clinical Trials. gov (ID: NCT02820974 ). Registration date: September 28th, 2014.

Keywords: Artery spin labeling (ASL); Diffusional kurtosis imaging (DKI); Functional connectivity (FC); Migraine; Multi-modal; Perimenopausal; Voxel-based morphology (VBM).

Conflict of interest statement

Ethics approval and consent to participate

The experiment conformed to the principles of the Declaration of Helsinki and was approved by the ethics committee of the second affiliated hospital (Tangdu Hospital) of Fourth Military Medical University (TDLL-2015133). All subjects will be provided informed, written consents after the study procedure has been fully explained in detail.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
The flowchart of the current trial

References

    1. Headache Classification Committee of the International Headache S: the international classification of headache disorders, 3rd edition (beta version). Cephalalgia 2013, 33(9):629–808.
    1. Leonardi M, Steiner TJ, Scher AT, Lipton RB. The global burden of migraine: measuring disability in headache disorders with WHO's classification of functioning, disability and health (ICF) J Headache Pain. 2005;6(6):429–440. doi: 10.1007/s10194-005-0252-4.
    1. Buse DC, Lipton RB. Global perspectives on the burden of episodic and chronic migraine. Cephalalgia. 2013;33(11):885–890. doi: 10.1177/0333102413477736.
    1. Burch RC, Loder S, Loder E, Smitherman TA. The prevalence and burden of migraine and severe headache in the United States: updated statistics from government health surveillance studies. Headache. 2015;55(1):21–34. doi: 10.1111/head.12482.
    1. Buse DC, Loder EW, Gorman JA, Stewart WF, Reed ML, Fanning KM, Serrano D, Lipton RB. Sex differences in the prevalence, symptoms, and associated features of migraine, probable migraine and other severe headache: results of the American migraine prevalence and prevention (AMPP) study. Headache. 2013;53(8):1278–1299. doi: 10.1111/head.12150.
    1. Chai NC, Peterlin BL, Calhoun AH. Migraine and estrogen. Curr Opin Neurol. 2014;27(3):315–324. doi: 10.1097/WCO.0000000000000091.
    1. MacGregor EA. Migraine, the menopause and hormone replacement therapy: a clinical review. J Fam Plann Reprod Health Care. 2007;33(4):245–249. doi: 10.1783/147118907782101986.
    1. Martin VT. Migraine and the menopausal transition. Neurol Sci. 2014;35(Suppl 1):65–69. doi: 10.1007/s10072-014-1745-1.
    1. Martin VT, Pavlovic J, Fanning KM, Buse DC, Reed ML, Lipton RB. Perimenopause and menopause are associated with high frequency headache in women with migraine: results of the American migraine prevalence and prevention study. Headache. 2016;56(2):292–305. doi: 10.1111/head.12763.
    1. Amandusson A, Blomqvist A. Estrogenic influences in pain processing. Front Neuroendocrinol. 2013;34(4):329–349. doi: 10.1016/j.yfrne.2013.06.001.
    1. Ibrahimi K, Couturier EG, MaassenVanDenBrink A. Migraine and perimenopause. Maturitas. 2014;78(4):277–280. doi: 10.1016/j.maturitas.2014.05.018.
    1. Macgregor EA. Perimenopausal migraine in women with vasomotor symptoms. Maturitas. 2012;71(1):79–82. doi: 10.1016/j.maturitas.2011.11.001.
    1. MacGregor EA. Estrogen replacement and migraine. Maturitas. 2009;63(1):51–55. doi: 10.1016/j.maturitas.2009.03.016.
    1. Shuster LT, Faubion SS, Sood R, Casey PM. Hormonal manipulation strategies in the management of menstrual migraine and other hormonally related headaches. Curr Neurol Neurosci Rep. 2011;11(2):131–138. doi: 10.1007/s11910-010-0174-7.
    1. Colombo B, Rocca MA, Messina R, Guerrieri S, Filippi M. Resting-state fMRI functional connectivity: a new perspective to evaluate pain modulation in migraine? Neurol Sci. 2015;36(Suppl 1):41–45. doi: 10.1007/s10072-015-2145-x.
    1. Chen Z, Chen X, Liu M, Liu S, Shu S, Ma L, Yu S. Altered functional connectivity of the marginal division in migraine: a resting-state fMRI study. J Headache Pain. 2016;17(1):89. doi: 10.1186/s10194-016-0682-1.
    1. Huang J, DeLano M, Cao Y. Visual cortical inhibitory function in migraine is not generally impaired: evidence from a combined psychophysical test with an fMRI study. Cephalalgia. 2006;26(5):554–560. doi: 10.1111/j.1468-2982.2006.01067.x.
    1. Maleki N, Linnman C, Brawn J, Burstein R, Becerra L, Borsook D. Her versus his migraine: multiple sex differences in brain function and structure. Brain. 2012;135(Pt 8):2546–2559. doi: 10.1093/brain/aws175.
    1. Kim JH, Suh SI, Seol HY, Oh K, Seo WK, Yu SW, Park KW, Koh SB. Regional grey matter changes in patients with migraine: a voxel-based morphometry study. Cephalalgia. 2008;28(6):598–604. doi: 10.1111/j.1468-2982.2008.01550.x.
    1. Huang Q, Lv X, He Y, Wei X, Ma M, Liao Y, Qin C, Wu Y. Structural differences in interictal migraine attack after epilepsy: a diffusion tensor imaging analysis. Epilepsy Behav. 2017;77:8–12. doi: 10.1016/j.yebeh.2017.09.002.
    1. Liu J, Zhao L, Lei F, Zhang Y, Yuan K, Gong Q, Liang F, Tian J. Disrupted resting-state functional connectivity and its changing trend in migraine suffers. Hum Brain Mapp. 2015;36(5):1892–1907. doi: 10.1002/hbm.22744.
    1. Alsop DC, Detre JA, Golay X, Gunther M, Hendrikse J, Hernandez-Garcia L, Lu H, MacIntosh BJ, Parkes LM, Smits M, et al. Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: a consensus of the ISMRM perfusion study group and the European consortium for ASL in dementia. Magn Reson Med. 2015;73(1):102–116. doi: 10.1002/mrm.25197.
    1. Rusinek H, Ha J, Yau PL, Storey P, Tirsi A, Tsui WH, Frosch O, Azova S, Convit A. Cerebral perfusion in insulin resistance and type 2 diabetes. J Cereb Blood Flow Metab. 2015;35(1):95–102. doi: 10.1038/jcbfm.2014.173.
    1. Hayes RB, Sigurdson A, Moore L, Peters U, Huang WY, Pinsky P, Reding D, Gelmann EP, Rothman N, Pfeiffer RM, et al. Methods for etiologic and early marker investigations in the PLCO trial. Mutat Res. 2005;592(1–2):147–154. doi: 10.1016/j.mrfmmm.2005.06.013.
    1. Smith SM. Fast robust automated brain extraction. Hum Brain Mapp. 2002;17(3):143–155. doi: 10.1002/hbm.10062.
    1. Ashburner J. A fast diffeomorphic image registration algorithm. NeuroImage. 2007;38(1):95. doi: 10.1016/j.neuroimage.2007.07.007.
    1. NeuroImage Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage. 2004;23(Suppl 1):S208–S219.
    1. Friston KJ, Williams S, Howard R, Frackowiak RS, Turner R. Movement-related effects in fMRI time-series. Magn Reson Med. 1996;35(3):346–355. doi: 10.1002/mrm.1910350312.
    1. Bullmore ET, Suckling J, Overmeyer S, Rabe-Hesketh S, Taylor E, Brammer MJ. Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Trans Med Imaging. 2002;18(1):32–42. doi: 10.1109/42.750253.
    1. Valfrè W, Rainero I, Bergui M, Pinessi L. Voxel-based morphometry reveals gray matter abnormalities in migraine. Headache the J Head & Face Pain. 2010;48(1):109–117. doi: 10.1111/j.1526-4610.2007.00723.x.
    1. Jin C, Yuan K, Zhao L, Zhao L, Yu D, Deneen KMV, Zhang M, Qin W, Sun W, Tian J. Structural and functional abnormalities in migraine patients without aura. NMR Biomed. 2013;26(1):58–64. doi: 10.1002/nbm.2819.
    1. Obermann M, Wurthmann S, Steinberg BS, Theysohn N, Diener HC, Naegel S. Central vestibular system modulation in vestibular migraine. Cephalalgia. 2014;34(13):1053–1061. doi: 10.1177/0333102414527650.
    1. Schmidtwilcke T, Gänssbauer S, Neuner T, Bogdahn U, May A. Subtle grey matter changes between migraine patients and healthy controls. Cephalalgia. 2008;28(1):1–4. doi: 10.1111/j.1468-2982.2007.01428.x.
    1. Russo A, Tessitore A, Giordano A, Corbo D, Marcuccio L, De SM, Salemi F, Conforti R, Esposito F, Tedeschi G. Executive resting-state network connectivity in migraine without aura. Cephalalgia. 2012;32(14):1041. doi: 10.1177/0333102412457089.
    1. Tessitore A, Russo A, Giordano A, Conte F, Corbo D, Stefano MD, Cirillo S, Cirillo M, Esposito F, Tedeschi G. Disrupted default mode network connectivity in migraine without aura. J Headache & Pain. 2013;14(1):1–7. doi: 10.1186/1129-2377-14-89.
    1. Dai Z, Zhong J, Xiao P, Zhu Y, Chen F, Pan P, Shi H. Gray matter correlates of migraine and gender effect: a meta-analysis of voxel-based morphometry studies. Neuroscience. 2015;299:88–96. doi: 10.1016/j.neuroscience.2015.04.066.
    1. Coppola G, Tinelli E, Lepre C, Iacovelli E, Di LC, Di LG, Serrao M, Pauri F, Fiermonte G, Bianco F. Dynamic changes in thalamic microstructure of migraine without aura patients: a diffusion tensor magnetic resonance imaging study. Eur J Neurol. 2014;21(2):287–e213. doi: 10.1111/ene.12296.
    1. Kara B, Kiyat AA, Onat L, Ulusoy L, Mutlu A, Sirvanci M. DTI findings during spontaneous migraine attacks. Clin Neuroradiol. 2013;23(1):31. doi: 10.1007/s00062-012-0165-y.
    1. Yu D, Yuan K, Zhao L, Dong M, Liu P, Yang X, Liu J, Sun J, Zhou G, Xue T. White matter integrity affected by depressive symptoms in migraine without aura: a tract-based spatial statistics study. NMR Biomed. 2013;26(9):1103–1112. doi: 10.1002/nbm.2924.
    1. Kai Y, Wei Q, Peng L, Ling Z, Yu D, Zhao L, Dong M, Liu J, Yang X, Deneen KMV. Reduced fractional anisotropy of Corpus callosum modulates inter-hemispheric resting state functional connectivity in migraine patients without Aura. PLoS One. 2012;7(9):e45476. doi: 10.1371/journal.pone.0045476.
    1. Rocca MA, Pagani E, Colombo B, Tortorella P, Falini A, Comi G, Filippi M. Selective diffusion changes of the visual pathways in patients with migraine: a 3-T tractography study. Cephalalgia. 2008;28(10):1061–1068. doi: 10.1111/j.1468-2982.2008.01655.x.
    1. Eidlitz-Markus T, Zeharia A, Haimi-Cohen Y, Konen O. MRI white matter lesions in pediatric migraine. Cephalalgia. 2013;33(11):906–913. doi: 10.1177/0333102413480955.
    1. Candee MS, McCandless RT, Moore KR, Arrington CB, Minich LL, Bale JF, Jr.: White matter lesions in children and adolescents with migraine. Pediatr Neurol 2013, 49(6):393–396.
    1. Mainero C, Boshyan J, Hadjikhani N. Altered functional magnetic resonance imaging resting-state connectivity in periaqueductal gray networks in migraine. Ann Neurol. 2011;70(5):838–845. doi: 10.1002/ana.22537.
    1. Tso AR, Trujillo A, Guo CC, Goadsby PJ, Seeley WW. The anterior insula shows heightened interictal intrinsic connectivity in migraine without aura. Neurology. 2015;84(10):1043–1050. doi: 10.1212/WNL.0000000000001330.
    1. Tessitore A, Russo A, Conte F, Giordano A, De Stefano M, Lavorgna L, Corbo D, Caiazzo G, Esposito F, Tedeschi G. Abnormal connectivity within executive resting-state network in migraine with Aura. Headache. 2015;55(6):794–805. doi: 10.1111/head.12587.
    1. Russo A, Marcelli V, Esposito F, Corvino V, Marcuccio L, Giannone A, Conforti R, Marciano E, Tedeschi G, Tessitore A. Abnormal thalamic function in patients with vestibular migraine. Neurology. 2014;82(23):2120–2126. doi: 10.1212/WNL.0000000000000496.
    1. Liu J, Zhao L, Li G, Xiong S, Nan J, Li J, Yuan K, von Deneen KM, Liang F, Qin W, et al. Hierarchical alteration of brain structural and functional networks in female migraine sufferers. PLoS One. 2012;7(12):e51250. doi: 10.1371/journal.pone.0051250.
    1. Nishimiya M, Matsuda H, Imabayashi E, Kuji I, Sato N. Comparison of SPM and NEUROSTAT in voxelwise statistical analysis of brain SPECT and MRI at the early stage of Alzheimer's disease. Ann Nucl Med. 2008;22(10):921–927. doi: 10.1007/s12149-008-0211-7.
    1. Ansar MA, Osaki Y, Kazui H, Oku N, Takasawa M, Kimura Y, Begum NN, Ikejiri Y, Takeda M, Hatazawa J. Effect of linearization correction on statistical parametric mapping (SPM): a 99mTc-HMPAO brain perfusion SPECT study in mild Alzheimer’s disease. Ann Nucl Med. 2006;20(8):511–517. doi: 10.1007/BF03026814.
    1. Youssef AM, Ludwick A, Wilcox SL, Lebel A, Peng K, Colon E, Danehy A, Burstein R, Becerra L, Borsook D. In child and adult migraineurs the somatosensory cortex stands out ... Again: an arterial spin labeling investigation. Hum Brain Mapp. 2017;38(8):4078–4087. doi: 10.1002/hbm.23649.
    1. Cadiot D, Longuet R, Bruneau B, Treguier C, Carsin-Vu A, Corouge I, Gomes C, Proisy M. Magnetic resonance imaging in children presenting migraine with aura: association of hypoperfusion detected by arterial spin labelling and vasospasm on MR angiography findings. Cephalalgia. 2018;38(5):949–958. doi: 10.1177/0333102417723570.
    1. Gil-Gouveia R, Pinto J, Figueiredo P, Vilela PF, Martins IP. An arterial spin labeling MRI perfusion study of migraine without Aura attacks. Front Neurol. 2017;8:280. doi: 10.3389/fneur.2017.00280.

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