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Published in: BMC Neurology 1/2018

Open Access 01-12-2018 | Research article

Right-to-left shunt and subclinical ischemic brain lesions in Chinese migraineurs: a multicentre MRI study

Authors: Xiao-han Jiang, Si-bo Wang, Qian Tian, Chi Zhong, Guan-ling Zhang, Ya-jie Li, Pan Lin, Yong You, Rong Guo, Ying-hua Cui, Ying-qi Xing

Published in: BMC Neurology | Issue 1/2018

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Abstract

Background

Migraine is considered as a risk factor for subclinical brain ischemic lesions, and right-to-left shunt (RLS) is more common among migraineurs. This cross-sectional study assessed the association of RLS with the increased prevalence of subclinical ischemic brain lesions in migraineurs.

Methods

We enrolled 334 migraineurs from a multicentre study from June 2015 to August 2016. Participants were all evaluated using contrast-enhanced transcranial Doppler, magnetic resonance imaging (MRI), and completed a questionnaire covering demographics, the main risk factors of vascular disease, and migraine status. RLS was classified into four grades (Grade 0 = Negative; Grade I = 1 ≤ microbubbles (MBs) ≤ 10; Grade II = MBs > 10 and no curtain; Grade III = curtain). Silent brain ischemic infarctions (SBI) and white matter hyperintensities (WMHs) were evaluated on MRI.

Results

We found no significant differences between migraineurs with RLS and migraineurs without RLS in subclinical ischemic brain lesions.SBI and WMHs did not increase with the size of the RLS(p for trend for SBI = 0.066, p for trend for WMHs = 0.543). Furthermore, curtain RLS in migraineurs was a risk factor for the presence of SBI (p = 0.032, OR = 3.47; 95%CI: 1.12−10.76). There was no association between RLS and the presence of WMHs.

Conclusion

Overall, RLS is not associated with increased SBI or WMHs in migraineurs. However, when RLS is present as a curtain pattern, it is likely to be a risk factor for SBIs in migraineurs.

Trial registration

No. NCT02425696; registered on April 21, 2015.
Appendix
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Literature
1.
go back to reference Kruit MC, van Buchem MA, Launer LJ, Terwindt GM, Ferrari MD. Migraine is associated with an increased risk of deep white matter lesions, subclinical posterior circulation infarcts and brain iron accumulation: the population-based MRI CAMERA study. Cephalalgia. 2010;30(2):129–36.CrossRefPubMedPubMedCentral Kruit MC, van Buchem MA, Launer LJ, Terwindt GM, Ferrari MD. Migraine is associated with an increased risk of deep white matter lesions, subclinical posterior circulation infarcts and brain iron accumulation: the population-based MRI CAMERA study. Cephalalgia. 2010;30(2):129–36.CrossRefPubMedPubMedCentral
2.
go back to reference Kurth T, Mohamed S, Maillard P, Zhu YC, Chabriat H, Mazoyer B, Bousser MG, Dufouil C, Tzourio C. Headache, migraine, and structural brain lesions and function: population based epidemiology of vascular ageing-MRI study. BMJ. 2011;342:c7357.CrossRefPubMedPubMedCentral Kurth T, Mohamed S, Maillard P, Zhu YC, Chabriat H, Mazoyer B, Bousser MG, Dufouil C, Tzourio C. Headache, migraine, and structural brain lesions and function: population based epidemiology of vascular ageing-MRI study. BMJ. 2011;342:c7357.CrossRefPubMedPubMedCentral
3.
go back to reference Ruchalla E. Migraine: structural brain changes in MRI. JAMA. 2013;185(12):1130. Ruchalla E. Migraine: structural brain changes in MRI. JAMA. 2013;185(12):1130.
4.
go back to reference Monteith T, Gardener H, Rundek T, Dong C, Yoshita M, Elkind MS, DeCarli C, Sacco RL, Wright CB. Migraine, white matter hyperintensities, and subclinical brain infarction in a diverse community: the northern Manhattan study. Stroke. 2014;45(6):1830–2.CrossRefPubMedPubMedCentral Monteith T, Gardener H, Rundek T, Dong C, Yoshita M, Elkind MS, DeCarli C, Sacco RL, Wright CB. Migraine, white matter hyperintensities, and subclinical brain infarction in a diverse community: the northern Manhattan study. Stroke. 2014;45(6):1830–2.CrossRefPubMedPubMedCentral
5.
go back to reference Koppen H, Palm-Meinders IH, Mess WH, Keunen RW, Terwindt GM, Launer LJ, van Buchem MA, Kruit MC, Ferrari MD. Systemic right-to-left shunts, ischemic brain lesions, and persistent migraine activity. Neurology. 2016;86(18):1668–75.CrossRefPubMedPubMedCentral Koppen H, Palm-Meinders IH, Mess WH, Keunen RW, Terwindt GM, Launer LJ, van Buchem MA, Kruit MC, Ferrari MD. Systemic right-to-left shunts, ischemic brain lesions, and persistent migraine activity. Neurology. 2016;86(18):1668–75.CrossRefPubMedPubMedCentral
6.
go back to reference Kruit MC, van Buchem MA, Hofman PA, Bakkers JT, Terwindt GM, Ferrari MD, Launer LJ. Migraine as a risk factor for subclinical brain lesions. JAMA. 2004;291(4):427–34.CrossRefPubMed Kruit MC, van Buchem MA, Hofman PA, Bakkers JT, Terwindt GM, Ferrari MD, Launer LJ. Migraine as a risk factor for subclinical brain lesions. JAMA. 2004;291(4):427–34.CrossRefPubMed
7.
go back to reference Scher AI, Gudmundsson LS, Sigurdsson S, Ghambaryan A, Aspelund T, Eiriksdottir G, van Buchem MA, Gudnason V, Launer LJ. Migraine headache in middle age and late-life brain infarcts. JAMA. 2009;301(24):2563–70.CrossRefPubMedPubMedCentral Scher AI, Gudmundsson LS, Sigurdsson S, Ghambaryan A, Aspelund T, Eiriksdottir G, van Buchem MA, Gudnason V, Launer LJ. Migraine headache in middle age and late-life brain infarcts. JAMA. 2009;301(24):2563–70.CrossRefPubMedPubMedCentral
8.
go back to reference Wilmshurst P, Nightingale S. Relationship between migraine and cardiac and pulmonary right-to-left shunts. Clin Sci (Lond). 2001;100(2):215–20.CrossRef Wilmshurst P, Nightingale S. Relationship between migraine and cardiac and pulmonary right-to-left shunts. Clin Sci (Lond). 2001;100(2):215–20.CrossRef
9.
go back to reference Domitrz I, Mieszkowski J, Kaminska A. Relationship between migraine and patent foramen ovale: a study of 121 patients with migraine. Headache. 2007;47(9):1311–8.CrossRefPubMed Domitrz I, Mieszkowski J, Kaminska A. Relationship between migraine and patent foramen ovale: a study of 121 patients with migraine. Headache. 2007;47(9):1311–8.CrossRefPubMed
10.
go back to reference Wammes-van der Heijden EA, Tijssen CC, Egberts AC. Right-to-left shunt and migraine: the strength of the relationship. Cephalalgia. 2006;26(2):208–13.CrossRefPubMed Wammes-van der Heijden EA, Tijssen CC, Egberts AC. Right-to-left shunt and migraine: the strength of the relationship. Cephalalgia. 2006;26(2):208–13.CrossRefPubMed
11.
go back to reference Anzola GP, Magoni M, Guindani M, Rozzini L, Dalla Volta G. Potential source of cerebral embolism in migraine with aura: a transcranial Doppler study. Neurology. 1999;52(8):1622–5.CrossRefPubMed Anzola GP, Magoni M, Guindani M, Rozzini L, Dalla Volta G. Potential source of cerebral embolism in migraine with aura: a transcranial Doppler study. Neurology. 1999;52(8):1622–5.CrossRefPubMed
12.
go back to reference Schwerzmann M, Nedeltchev K, Lagger F, Mattle HP, Windecker S, Meier B, Seiler C. Prevalence and size of directly detected patent foramen ovale in migraine with aura. Neurology. 2005;65(9):1415–8.CrossRefPubMed Schwerzmann M, Nedeltchev K, Lagger F, Mattle HP, Windecker S, Meier B, Seiler C. Prevalence and size of directly detected patent foramen ovale in migraine with aura. Neurology. 2005;65(9):1415–8.CrossRefPubMed
13.
go back to reference Xu WH, Xing YQ, Yan ZR, Jiang JD, Gao S. Cardiac right-to-left shunt subtypes in Chinese patients with cryptogenic strokes: a multicenter case-control study. Eur J Neurol. 2014;21(3):525–8.CrossRefPubMed Xu WH, Xing YQ, Yan ZR, Jiang JD, Gao S. Cardiac right-to-left shunt subtypes in Chinese patients with cryptogenic strokes: a multicenter case-control study. Eur J Neurol. 2014;21(3):525–8.CrossRefPubMed
14.
go back to reference Hao N, Liu K, Guo ZN, Wu X, Yang Y, Xing Y. Comparison of two contrast agents for right-to-left shunt diagnosis with contrast-enhanced transcranial Doppler. Ultrasound Med Biol. 2014;40(9):2317–20.CrossRefPubMed Hao N, Liu K, Guo ZN, Wu X, Yang Y, Xing Y. Comparison of two contrast agents for right-to-left shunt diagnosis with contrast-enhanced transcranial Doppler. Ultrasound Med Biol. 2014;40(9):2317–20.CrossRefPubMed
15.
go back to reference Yang Y, Guo ZN, Wu J, Jin H, Wang X, Xu J, Feng J, Xing Y. Prevalence and extent of right-to-left shunt in migraine: a survey of 217 Chinese patients. Eur J Neurol. 2012;19(10):1367–72.CrossRefPubMed Yang Y, Guo ZN, Wu J, Jin H, Wang X, Xu J, Feng J, Xing Y. Prevalence and extent of right-to-left shunt in migraine: a survey of 217 Chinese patients. Eur J Neurol. 2012;19(10):1367–72.CrossRefPubMed
16.
go back to reference Serena J, Segura T, Perez-Ayuso MJ, Bassaganyas J, Molins A, Davalos A. The need to quantify right-to-left shunt in acute ischemic stroke: a case-control study. Stroke. 1998;29(7):1322–8.CrossRefPubMed Serena J, Segura T, Perez-Ayuso MJ, Bassaganyas J, Molins A, Davalos A. The need to quantify right-to-left shunt in acute ischemic stroke: a case-control study. Stroke. 1998;29(7):1322–8.CrossRefPubMed
17.
go back to reference Jauss M, Zanette E. Detection of right-to-left shunt with ultrasound contrast agent and transcranial Doppler sonography. Cerebrovasc Dis. 2000;10(6):490–6.CrossRefPubMed Jauss M, Zanette E. Detection of right-to-left shunt with ultrasound contrast agent and transcranial Doppler sonography. Cerebrovasc Dis. 2000;10(6):490–6.CrossRefPubMed
18.
go back to reference Gaist D, Garde E, Blaabjerg M, Nielsen HH, Kroigard T, Ostergaard K, Moller HS, Hjelmborg J, Madsen CG, Iversen P, et al. Migraine with aura and risk of silent brain infarcts and white matter hyperintensities: an MRI study. Brain. 2016;139(Pt 7):2015–23.CrossRefPubMedPubMedCentral Gaist D, Garde E, Blaabjerg M, Nielsen HH, Kroigard T, Ostergaard K, Moller HS, Hjelmborg J, Madsen CG, Iversen P, et al. Migraine with aura and risk of silent brain infarcts and white matter hyperintensities: an MRI study. Brain. 2016;139(Pt 7):2015–23.CrossRefPubMedPubMedCentral
20.
go back to reference Del Zotto E, Pezzini A, Giossi A, Volonghi I, Padovani A. Migraine and ischemic stroke: a debated question. J Cereb Blood Flow Metab. 2008;28(8):1399–421.CrossRefPubMed Del Zotto E, Pezzini A, Giossi A, Volonghi I, Padovani A. Migraine and ischemic stroke: a debated question. J Cereb Blood Flow Metab. 2008;28(8):1399–421.CrossRefPubMed
21.
go back to reference Bednarczyk EM, Remler B, Weikart C, Nelson AD, Reed RC. Global cerebral blood flow, blood volume, and oxygen metabolism in patients with migraine headache. Neurology. 1998;50(6):1736–40.CrossRefPubMed Bednarczyk EM, Remler B, Weikart C, Nelson AD, Reed RC. Global cerebral blood flow, blood volume, and oxygen metabolism in patients with migraine headache. Neurology. 1998;50(6):1736–40.CrossRefPubMed
22.
go back to reference Calviere L, Tall P, Massabuau P, Bonneville F, Larrue V. Migraine with aura and silent brain infarcts lack of mediation of patent foramen ovale. Eur J Neurol. 2013;20(12):1560–5.CrossRefPubMed Calviere L, Tall P, Massabuau P, Bonneville F, Larrue V. Migraine with aura and silent brain infarcts lack of mediation of patent foramen ovale. Eur J Neurol. 2013;20(12):1560–5.CrossRefPubMed
23.
go back to reference Guo ZN, Xing Y, Liu J, Wang S, Yan S, Jin H, Yang Y. Compromised dynamic cerebral autoregulation in patients with a right-to-left shunt: a potential mechanism of migraine and cryptogenic stroke. PLoS One. 2014;9(8):e104849.CrossRefPubMedPubMedCentral Guo ZN, Xing Y, Liu J, Wang S, Yan S, Jin H, Yang Y. Compromised dynamic cerebral autoregulation in patients with a right-to-left shunt: a potential mechanism of migraine and cryptogenic stroke. PLoS One. 2014;9(8):e104849.CrossRefPubMedPubMedCentral
24.
go back to reference Rigatelli G, Dell'Avvocata F, Cardaioli P, Giordan M, Braggion G, Aggio S, Chinaglia M, Mandapaka S, Kuruvilla J, Chen JP, et al. Permanent right-to-left shunt is the key factor in managing patent foramen ovale. J Am Coll Cardiol. 2011;58(21):2257–61.CrossRefPubMed Rigatelli G, Dell'Avvocata F, Cardaioli P, Giordan M, Braggion G, Aggio S, Chinaglia M, Mandapaka S, Kuruvilla J, Chen JP, et al. Permanent right-to-left shunt is the key factor in managing patent foramen ovale. J Am Coll Cardiol. 2011;58(21):2257–61.CrossRefPubMed
25.
go back to reference Kruit MC, Launer LJ, Ferrari MD, van Buchem MA. Infarcts in the posterior circulation territory in migraine. The population-based MRI CAMERA study. Brain. 2005;128(Pt 9):2068–77.CrossRefPubMed Kruit MC, Launer LJ, Ferrari MD, van Buchem MA. Infarcts in the posterior circulation territory in migraine. The population-based MRI CAMERA study. Brain. 2005;128(Pt 9):2068–77.CrossRefPubMed
26.
go back to reference Feurer R, Sadikovic S, Esposito L, Schwarze J, Bockelbrink A, Hemmer B, Sander D, Poppert H. Lesion patterns in patients with cryptogenic stroke with and without right-to-left-shunt. Eur J Neurol. 2009;16(10):1077–82.CrossRefPubMed Feurer R, Sadikovic S, Esposito L, Schwarze J, Bockelbrink A, Hemmer B, Sander D, Poppert H. Lesion patterns in patients with cryptogenic stroke with and without right-to-left-shunt. Eur J Neurol. 2009;16(10):1077–82.CrossRefPubMed
27.
go back to reference Swartz RH, Kern RZ. Migraine is associated with magnetic resonance imaging white matter abnormalities: a meta-analysis. Arch Neurol. 2004;61(9):1366–8.CrossRefPubMed Swartz RH, Kern RZ. Migraine is associated with magnetic resonance imaging white matter abnormalities: a meta-analysis. Arch Neurol. 2004;61(9):1366–8.CrossRefPubMed
28.
go back to reference Del Sette M, Dinia L, Bonzano L, Roccatagliata L, Finocchi C, Parodi RC, Sivori G, Gandolfo C. White matter lesions in migraine and right-to-left shunt: a conventional and diffusion MRI study. Cephalalgia. 2008;28(4):376–82.CrossRefPubMed Del Sette M, Dinia L, Bonzano L, Roccatagliata L, Finocchi C, Parodi RC, Sivori G, Gandolfo C. White matter lesions in migraine and right-to-left shunt: a conventional and diffusion MRI study. Cephalalgia. 2008;28(4):376–82.CrossRefPubMed
29.
go back to reference Park HK, Lee SY, Kim SE, Yun CH, Kim SH. Small deep white matter lesions are associated with right-to-left shunts in migraineurs. J Neurol. 2011;258(3):427–33.CrossRefPubMed Park HK, Lee SY, Kim SE, Yun CH, Kim SH. Small deep white matter lesions are associated with right-to-left shunts in migraineurs. J Neurol. 2011;258(3):427–33.CrossRefPubMed
30.
go back to reference Rigatelli G, Cardaioli P, Dell'Avvocata F, Giordan M, Braggion G, Chinaglia M, Roncon L. Transcatheter patent foramen ovale closure is effective in reducing migraine independently from specific interatrial septum anatomy and closure devices design. Cardiovasc Revasc Med. 2010;11(1):29–33.CrossRefPubMed Rigatelli G, Cardaioli P, Dell'Avvocata F, Giordan M, Braggion G, Chinaglia M, Roncon L. Transcatheter patent foramen ovale closure is effective in reducing migraine independently from specific interatrial septum anatomy and closure devices design. Cardiovasc Revasc Med. 2010;11(1):29–33.CrossRefPubMed
31.
go back to reference Wahl A, Kunz M, Moschovitis A, Nageh T, Schwerzmann M, Seiler C, Mattle HP, Windecker S, Meier B. Long-term results after fluoroscopy-guided closure of patent foramen ovale for secondary prevention of paradoxical embolism. Heart. 2008;94(3):336–41.CrossRefPubMed Wahl A, Kunz M, Moschovitis A, Nageh T, Schwerzmann M, Seiler C, Mattle HP, Windecker S, Meier B. Long-term results after fluoroscopy-guided closure of patent foramen ovale for secondary prevention of paradoxical embolism. Heart. 2008;94(3):336–41.CrossRefPubMed
32.
go back to reference Wahl A, Praz F, Tai T, Findling O, Walpoth N, Nedeltchev K, Schwerzmann M, Windecker S, Mattle HP, Meier B. Improvement of migraine headaches after percutaneous closure of patent foramen ovale for secondary prevention of paradoxical embolism. Heart. 2010;96(12):967–73.CrossRefPubMed Wahl A, Praz F, Tai T, Findling O, Walpoth N, Nedeltchev K, Schwerzmann M, Windecker S, Mattle HP, Meier B. Improvement of migraine headaches after percutaneous closure of patent foramen ovale for secondary prevention of paradoxical embolism. Heart. 2010;96(12):967–73.CrossRefPubMed
33.
go back to reference Meier B, Kalesan B, Mattle HP, Khattab AA, Hildick-Smith D, Dudek D, Andersen G, Ibrahim R, Schuler G, Walton AS, et al. Percutaneous closure of patent foramen ovale in cryptogenic embolism. N Engl J Med. 2013;368(12):1083–91.CrossRefPubMed Meier B, Kalesan B, Mattle HP, Khattab AA, Hildick-Smith D, Dudek D, Andersen G, Ibrahim R, Schuler G, Walton AS, et al. Percutaneous closure of patent foramen ovale in cryptogenic embolism. N Engl J Med. 2013;368(12):1083–91.CrossRefPubMed
34.
go back to reference Wolfrum M, Froehlich GM, Knapp G, Casaubon LK, DiNicolantonio JJ, Lansky AJ, Meier P. Stroke prevention by percutaneous closure of patent foramen ovale: a systematic review and meta-analysis. Heart. 2014;100(5):389–95.CrossRefPubMed Wolfrum M, Froehlich GM, Knapp G, Casaubon LK, DiNicolantonio JJ, Lansky AJ, Meier P. Stroke prevention by percutaneous closure of patent foramen ovale: a systematic review and meta-analysis. Heart. 2014;100(5):389–95.CrossRefPubMed
Metadata
Title
Right-to-left shunt and subclinical ischemic brain lesions in Chinese migraineurs: a multicentre MRI study
Authors
Xiao-han Jiang
Si-bo Wang
Qian Tian
Chi Zhong
Guan-ling Zhang
Ya-jie Li
Pan Lin
Yong You
Rong Guo
Ying-hua Cui
Ying-qi Xing
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Neurology / Issue 1/2018
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/s12883-018-1022-7

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