Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
The Journal of Headache and Pain
Published in: The Journal of Headache and Pain 1/2021

Open Access 01-12-2021 | Migraine | Research article

Assessment of normalized cerebral blood flow and its connectivity with migraines without aura during interictal periods by arterial spin labeling

Authors: Di Zhang, Xiaobin Huang, Cunnan Mao, Yuchen Chen, Zhengfei Miao, Chunmei Liu, Chenjie Xu, Xinying Wu, Xindao Yin

Published in: The Journal of Headache and Pain | Issue 1/2021

Login to get access

Abstract

Background

Migraine constitutes a global health burden, and its pathophysiology is not well-understood; research evaluating cerebral perfusion and altered blood flow between brain areas using non-invasive imaging techniques, such as arterial spin labeling, have been scarce. This study aimed to assess cerebral blood flow (CBF) and its connectivity of migraine.

Methods

This study enrolled 40 patients with episodic migraine without aura (MwoA), as well as 42 healthy patients as control (HC). Two groups of normalized CBF and CBF connectivity were compared, and the relationship between CBF variation and clinical scale assessment was further evaluated.

Results

In comparison to HC subjects, MwoA patients exhibited higher CBF in the right middle frontal orbital gyrus (ORBmid.R) and the right middle frontal gyrus, while that in Vermis_6 declined. The increased CBF of ORBmid.R was positively correlated with both the Visual Light Sensitivity Questionnaire-8 (VLSQ-8) and the monthly attack frequency score. In MwoA, significantly decreased CBF connectivity was detected between ORBmid.R and the left superior frontal gyrus, the right putamen, the right caudate, as well as the right angular gyrus. In addition, increased CBF connectivity was observed between the left calcarine cortex and ORBmid.R.

Conclusions

Our results indicate that migraine patients exhibit abnormalities in regional CBF and feature CBF connection defects at the resting state. The affected areas involve information perception, information integration, and emotional, pain and visual processing. Our findings might provide important clues for the pathophysiology of migraine.
Literature
1.
Group GBDNDC (2017) Global, regional, and national burden of neurological disorders during 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet Neurol 16:877–897CrossRef
2.
Roncolato M, Fabbri L, Recchia G, Cavazzuti L, Visona G, Brignoli O, Medea G (2000) An epidemiological study to assess migraine prevalence in a sample of Italian population presenting to their GPs. Eur Neurol 43:102–106PubMedCrossRef
3.
4.
Solstrand Dahlberg L, Linnman CN, Lee D, Burstein R, Becerra L, Borsook D (2018) Responsivity of periaqueductal gray connectivity is related to headache frequency in episodic migraine. Front Neurol 9:61PubMedPubMedCentralCrossRef
5.
Yu ZB, Lv YB, Song LH, Liu DH, Huang XL, Hu XY, Zuo ZW, Wang Y, Yang Q, Peng J, Zhou ZH, Li HT (2017) Functional connectivity differences in the insular sub-regions in migraine without aura: a resting-state functional magnetic resonance imaging study. Front Behav Neurosci 11:124PubMedPubMedCentralCrossRef
6.
Gaist D, Hougaard A, Garde E, Reislev NL, Wiwie R, Iversen P, Madsen CG, Blaabjerg M, Nielsen HH, Kroigard T, Ostergaard K, Kyvik KO, Hjelmborg J, Madsen K, Siebner HR, Ashina M (2018) Migraine with visual aura associated with thicker visual cortex. Brain 141:776–785PubMedCrossRef
7.
Michelle Welman FHS, Smit AE, Jongen JLM, Tibboel D, van der Geest JN, Holstege JC (2018) Pain experience is somatotopically organized and overlaps with pain anticipation in the human cerebellum. Cerebellum 17:447–460PubMedPubMedCentralCrossRef
8.
Huang X, Zhang D, Chen Y, Wang P, Mao C, Miao Z, Liu C, Xu C, Wu X, Yin X (2019) Altered functional connectivity of the red nucleus and substantia nigra in migraine without aura. J Headache Pain 20:104PubMedPubMedCentralCrossRef
9.
Russo A, Tessitore A, Silvestro M, Di Nardo F, Trojsi F, Del Santo T, De Micco R, Esposito F, Tedeschi G (2019) Advanced visual network and cerebellar hyperresponsiveness to trigeminal nociception in migraine with aura. J Headache Pain 20:46PubMedPubMedCentralCrossRef
10.
Zhang D, Huang X, Su W, Chen Y, Wang P, Mao C, Miao Z, Liu C, Xu C, Yin X, Wu X (2020) Altered lateral geniculate nucleus functional connectivity in migraine without aura: a resting-state functional MRI study. J Headache Pain 21:17PubMedPubMedCentralCrossRef
11.
Shin JH, Kim YK, Kim HJ, Kim JS (2014) Altered brain metabolism in vestibular migraine: comparison of interictal and ictal findings. Cephalalgia 34:58–67PubMedCrossRef
12.
Cadiot D, Longuet R, Bruneau B, Treguier C, Carsin-Vu A, Corouge I, Gomes C, Proisy M (2018) Magnetic resonance imaging in children presenting migraine with aura: association of hypoperfusion detected by arterial spin labelling and vasospasm on MR angiography findings. Cephalalgia 38:949–958PubMedCrossRef
13.
Miller C, Goldberg MF (2012) Susceptibility-weighted imaging and computed tomography perfusion abnormalities in diagnosis of classic migraine. Emerg Radiol 19:565–569PubMedCrossRef
14.
15.
Telischak NA, Detre JA, Zaharchuk G (2015) Arterial spin labeling MRI: clinical applications in the brain. J Magn Reson Imaging 41:1165–1180PubMedCrossRef
16.
Wolf ME, Okazaki S, Eisele P, Rossmanith C, Gregori J, Griebe M, Gunther M, Gass A, Hennerici MG, Szabo K, Kern R (2018) Arterial spin labeling cerebral perfusion magnetic resonance imaging in migraine aura: an observational study. J Stroke Cerebrovasc Dis 27:1262–1266PubMedCrossRef
17.
Xu G, Rowley HA, Wu G, Alsop DC, Shankaranarayanan A, Dowling M, Christian BT, Oakes TR, Johnson SC (2010) Reliability and precision of pseudo-continuous arterial spin labeling perfusion MRI on 3.0 T and comparison with 15O-water PET in elderly subjects at risk for Alzheimer’s disease. NMR Biomed 23:286–293
18.
Havsteen I, Damm Nybing J, Christensen H, Christensen AF (2018) Arterial spin labeling: a technical overview. Acta Radiol 59:1232–1238PubMedCrossRef
19.
Hernandez-Garcia L, Lahiri A, Schollenberger J (2019) Recent progress in ASL. Neuroimage 187:3–16PubMedCrossRef
20.
Floery D, Vosko MR, Fellner FA, Fellner C, Ginthoer C, Gruber F, Ransmayr G, Doerfler A, Uder M, Bradley WG (2012) Acute-onset migrainous aura mimicking acute stroke: MR perfusion imaging features. AJNR Am J Neuroradiol 33:1546–1552PubMedPubMedCentralCrossRef
21.
Linn J, Freilinger T, Morhard D, Bruckmann H, Straube A (2007) Aphasic migraineous aura with left parietal hypoperfusion: a case report. Cephalalgia 27:850–853PubMedCrossRef
22.
Oberndorfer S, Wober C, Nasel C, Asenbaum S, Lahrmann H, Fueger B, Grisold W (2004) Familial hemiplegic migraine: follow-up findings of diffusion-weighted magnetic resonance imaging (MRI), perfusion-MRI and [99mTc] HMPAO-SPECT in a patient with prolonged hemiplegic aura. Cephalalgia 24:533–539PubMedCrossRef
23.
Jacob A, Mahavish K, Bowden A, Smith ET, Enevoldson P, White RP (2006) Imaging abnormalities in sporadic hemiplegic migraine on conventional MRI, diffusion and perfusion MRI and MRS. Cephalalgia 26:1004–1009PubMedCrossRef
24.
Mourand I, Menjot de Champfleur N, Carra-Dalliere C, Le Bars E, Roubertie A, Bonafe A, Thouvenot E (2012) Perfusion-weighted MR imaging in persistent hemiplegic migraine. Neuroradiology 54:255–260PubMedCrossRef
25.
Meylakh N, Marciszewski KK, Di Pietro F, Macefield VG, Macey PM, Henderson LA (2020) Altered regional cerebral blood flow and hypothalamic connectivity immediately prior to a migraine headache. Cephalalgia 40:448–460PubMedCrossRef
26.
Corno S, Giani L, Lagana MM, Baglio F, Mariani C, Pantoni L, Lovati C (2018) The brain effect of the migraine attack: an ASL MRI study of the cerebral perfusion during a migraine attack. Neurol Sci 39:73–74PubMedCrossRef
27.
Younis S, Christensen CE, Vestergaard MB, Lindberg U, Tolnai D, Paulson OB, Larsson HB, Hougaard A, Ashina M (2020) Glutamate levels and perfusion in pons during migraine attacks: a 3T MRI study using proton spectroscopy and arterial spin labeling. J Cereb Blood Flow Metab 41(3):604–616
28.
Gil-Gouveia R, Pinto J, Figueiredo P, Vilela PF, Martins IP (2017) An arterial spin labeling MRI perfusion study of migraine without aura attacks. Front Neurol 8:280PubMedPubMedCentralCrossRef
29.
Li F, Lu L, Shang S, Chen H, Wang P, Haidari NA, Chen YC, Yin X (2020) Cerebral blood flow and its connectivity deficits in mild traumatic brain injury at the acute stage. Neural Plast 2020:2174371PubMedPubMedCentralCrossRef
30.
Shang SA, Wu J, Zhang H, Chen H, Cao Z, Chen YC, Yin X (2020) Motor asymmetry related cerebral perfusion patterns in Parkinson’s disease: an arterial spin labeling study. Hum Brain Mapp 42:298–309
31.
Melie-Garcia L, Sanabria-Diaz G, Sanchez-Catasus C (2013) Studying the topological organization of the cerebral blood flow fluctuations in resting state. Neuroimage 64:173–184PubMedCrossRef
32.
Mungoven TJ, Meylakh N, Marciszewski KK, Macefield VG, Macey PM, Henderson LA (2020) Microstructural changes in the trigeminal nerve of patients with episodic migraine assessed using magnetic resonance imaging. J Headache Pain 21:59PubMedPubMedCentralCrossRef
33.
Rudebeck PH, Murray EA (2014) The orbitofrontal oracle: cortical mechanisms for the prediction and evaluation of specific behavioral outcomes. Neuron 84:1143–1156PubMedPubMedCentralCrossRef
34.
Jonker FA, Jonker C, Scheltens P, Scherder EJ (2015) The role of the orbitofrontal cortex in cognition and behavior. Rev Neurosci 26:1–11PubMedCrossRef
35.
36.
Wang JJ, Chen X, Sah SK, Zeng C, Li YM, Li N, Liu MQ, Du SL (2016) Amplitude of low-frequency fluctuation (ALFF) and fractional ALFF in migraine patients: a resting-state functional MRI study. Clin Radiol 71:558–564PubMedCrossRef
37.
Jin L, Yang X, Liu P, Sun J, Chen F, Xu Z, Qin W, Tian J (2017) Dynamic abnormalities of spontaneous brain activity in women with primary dysmenorrhea. J Pain Res 10:699–707PubMedPubMedCentralCrossRef
38.
Cavada C, Company T, Tejedor J, Cruz-Rizzolo RJ, Reinoso-Suarez F (2000) The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cereb Cortex 10:220–242PubMedCrossRef
39.
Rocca MA, Messina R, Colombo B, Falini A, Comi G, Filippi M (2014) Structural brain MRI abnormalities in pediatric patients with migraine. J Neurol 261:350–357PubMedCrossRef
40.
Neeb L, Bastian K, Villringer K, Israel H, Reuter U, Fiebach JB (2017) Structural gray matter alterations in chronic migraine: implications for a progressive disease? Headache 57:400–416PubMedCrossRef
41.
de Pasquale F, Della Penna S, Snyder AZ, Marzetti L, Pizzella V, Romani GL, Corbetta M (2012) A cortical core for dynamic integration of functional networks in the resting human brain. Neuron 74:753–764PubMedPubMedCentralCrossRef
42.
Lo Buono V, Bonanno L, Corallo F, Pisani LR, Lo Presti R, Grugno R, Di Lorenzo G, Bramanti P, Marino S (2017) Functional connectivity and cognitive impairment in migraine with and without aura. J Headache Pain 18:72PubMedPubMedCentralCrossRef
43.
Aldusary N, Traber GL, Freund P, Fierz FC, Weber KP, Baeshen A, Alghamdi J, Saliju B, Pazahr S, Mazloum R, Alshehri F, Landau K, Kollias S, Piccirelli M, Michels L (2020) Abnormal connectivity and brain structure in patients with visual snow. Front Hum Neurosci 14:582031PubMedPubMedCentralCrossRef
44.
Johns P (2014) Clinical neuroscience. Churchill Livingstone, London
45.
Wei HL, Zhou X, Chen YC, Yu YS, Guo X, Zhou GP, Zhou QQ, Qu LJ, Yin X, Li J, Zhang H (2019) Impaired intrinsic functional connectivity between the thalamus and visual cortex in migraine without aura. J Headache Pain 20:116PubMedPubMedCentralCrossRef
46.
Liu H-Y, Lee P-L, Chou K-H, Lai K-L, Wang Y-F, Chen S-P, Chen W-T, Wang S-J (2020) The cerebellum is associated with 2-year prognosis in patients with high-frequency migraine. J Headache Pain 21:29PubMedPubMedCentralCrossRef
47.
Ohmura K, Suzuki Y, Saito Y, Wada T, Goto M, Seto S (2012) Sporadic hemiplegic migraine presenting as acute encephalopathy. Brain Dev 34:691–695PubMedCrossRef
48.
Yabe I, Kitagawa M, Suzuki Y, Fujiwara K, Wada T, Tsubuku T, Takeichi N, Sakushima K, Soma H, Tsuji S, Niino M, Saitoh S, Sasaki H (2008) Downbeat positioning nystagmus is a common clinical feature despite variable phenotypes in an FHM1 family. J Neurol 255:1541–1544PubMedCrossRef
49.
Dichgans M, Herzog J, Freilinger T, Wilke M, Auer DP (2005) 1H-MRS alterations in the cerebellum of patients with familial hemiplegic migraine type 1. Neurology 64:608–613PubMedCrossRef
Metadata
Title
Assessment of normalized cerebral blood flow and its connectivity with migraines without aura during interictal periods by arterial spin labeling
Authors
Di Zhang
Xiaobin Huang
Cunnan Mao
Yuchen Chen
Zhengfei Miao
Chunmei Liu
Chenjie Xu
Xinying Wu
Xindao Yin
Publication date
01-12-2021
Publisher
Springer Milan
Keywords
Migraine
Aura
Published in
The Journal of Headache and Pain / Issue 1/2021
Print ISSN: 1129-2369
Electronic ISSN: 1129-2377
DOI
https://doi.org/10.1186/s10194-021-01282-y

Other articles of this Issue 1/2021

The Journal of Headache and Pain 1/2021 Go to the issue

Research article

In search of a gold standard patient-reported outcome measure to use in the evaluation and treatment-decision making in migraine prevention. A real-world evidence study

Research article

Investigation of cortical thickness and volume during spontaneous attacks of migraine without aura: a 3-Tesla MRI study

Review article

Manual joint mobilisation techniques, supervised physical activity, psychological treatment, acupuncture and patient education for patients with tension-type headache. A systematic review and meta-analysis

Research article

A universal outcome measure for headache treatments, care-delivery systems and economic analysis

Research article

Long term safety, tolerability, and efficacy of intracutaneous zolmitriptan (M207) in the acute treatment of migraine

Research article

Mild traumatic brain injury affects the features of migraine