Skip to main content

Advertisement

SpringerLink
Log in

Completeness of circle of Willis and white matter hyperintensities in patients with severe internal carotid artery stenosis

  • Original Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

Background

We investigated whether completeness of the circle of Willis (CoW) protected patients with severe internal carotid artery (ICA) stenosis against white matter hyperintensities (WMHs).

Methods

We included 115 patients with unilateral ICA stenosis ≥ 70%. The completeness of CoW was assessed and WMHs were rated on a visual scale. The score of deep and periventricular WMHs was compared between patients with complete and incomplete CoW and between the two hemispheres, ipsilateral and contralateral to stenosed ICA.

Results

We included 115 patients with severe ICA stenosis, 60 patients had a complete CoW (52.17%) and 55 had an incomplete CoW (47.83%). The patients with incomplete CoW had higher score of deep WMHs (OR = 1.82, 95% CI 1.08–3.06, P = 0.023) and periventricular WMHs (OR = 4.53, 95% CI 2.09–9.81, P = 0.000) than those with complete CoW. In the patients with incomplete CoW, the score of deep WMHs (OR = 4.14, 95% CI 1.33–12.93, P = 0.014) and periventricular WMHs (OR = 5.46, 95% CI 1.16–25.62, P = 0.032) was higher in the hemisphere ipsilateral to stenosed ICA than that in the contralateral hemisphere. In the patients with complete CoW, there was no significant difference in the score of deep WMHs (OR = 2.10, 95% CI 0.37–11.91, P = 0.401) and periventricular WMHs (OR = 2.83, 95% CI 0.99–8.05, P = 0.051) between the ipsilateral and contralateral hemispheres to stenosed ICA.

Conclusion

The completeness of CoW protected patients with severe ICA stenosis against WMHs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Vernooij MW, Ikram MA, Tanghe HL, Vincent AJ, Hofman A, Krestin GP, Niessen WJ, Breteler MM, van der Lugt A (2007) Incidental findings on brain MRI in the general population. N Engl J Med 357:1821–1828

    Article  CAS  PubMed  Google Scholar 

  2. Smith EE, Saposnik G, Biessels GJ, Doubal FN, Fornage M, Gorelick PB, Greenberg SM, Higashida RT, Kasner SE, Seshadri S, American Heart Association Stroke Council; Council on Cardiovascular Radiology and Intervention; Council on Functional Genomics and Translational Biology; and Council on Hypertension (2017) Prevention of stroke in patients with silent cerebrovascular disease: a scientific statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 48:e44–e71

    PubMed  Google Scholar 

  3. Debette S, Markus HS (2010) The clinical importance of white matter hyperintensities on brain magnetic resonance imaging: systematic review and meta-analysis. BMJ 341:c3666

    Article  PubMed  PubMed Central  Google Scholar 

  4. Tang WK, Liang HJ, Chen YK, Ahuja AT, Chu WCW, Mok VCT, Ungvari GS, Wong KS (2013) White matter hyperintensities and quality of life in acute lacunar stroke. Neurol Sci 34:1347–1353

    Article  CAS  PubMed  Google Scholar 

  5. The LADIS Study Group, Poggesi A, Pantoni L, Inzitari D, Fazekas F, Ferro J, O'Brien J, Hennerici M, Scheltens P, Erkinjuntti T, Visser M, Langhorne P, Chabriat H, Waldemar G, Wallin A, Wahlund A (2011) 2001-2011: a decade of the LADIS (Leukoaraiosis and disability) study: what have we learned about white matter changes and small-vessel disease? Cerebrovasc Dis 32:577–588

    Article  Google Scholar 

  6. Ben-Assayag E, Mijajlovic M, Shenhar-Tsarfaty S, Bova I, Shopin L, Bornstein NM (2012) Leukoaraiosis is a chronic atherosclerotic disease. Sci World J 2012:6. https://doi.org/10.1100/2012/532141

  7. Ye H, Wang Y, Qiu J, Wu Q, Xu M, Wang J (2018) White matter hyperintensities and their subtypes in patients with carotid artery stenosis: a systematic review and meta-analysis. BMJ Open 8:e020830

    Article  PubMed  PubMed Central  Google Scholar 

  8. Saba L, Sanfilippo R, Pascalis L, Montisci R, Mallarini G (2009) Carotid artery abnormalities and leukoaraiosis in elderly patients: evaluation with MDCT. Am J Roentgenol 192:W63–W70

    Article  Google Scholar 

  9. Enzinger C, Ropele S, Gattringer T, Langkammer C, Schmidt R, Fazekas F (2010) High-grade internal carotid artery stenosis and chronic brain damage: a volumetric magnetic resonance imaging study. Cerebrovasc Dis 30:540–546

    Article  PubMed  Google Scholar 

  10. Hoksbergen AW, Majoie CB, Hulsmans FJ, Legemate DA (2013) Assessment of the collateral function of the circle of Willis: three-dimensional time-of-flight MR angiography compared with transcranial color coded duplex sonography. Am J Neuroradiol 24:456–462

    Google Scholar 

  11. Adams HP Jr, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, Marsh EE 3rd (1993) Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of org 10172 in acute stroke treatment. Stroke 24:35–41

    Article  PubMed  Google Scholar 

  12. Kim KW, MacFall JR, Payne ME (2008) Classification of white matter lesions on magnetic resonance imaging in elderly persons. Biol Psychiatry 64:273–280

    Article  PubMed  PubMed Central  Google Scholar 

  13. King KS, Peshock RM, Warren MW, Alhilali L, Hulsey K, McColl R, Weiner MF, Ayers C, Whittemore A (2013) Evaluation of a practical visual MRI rating scale of brain white matter hyperintensities for clinicians based on largest lesion size regardless of location. AJNR Am J Neuroradiol 34:797–801

    Article  CAS  PubMed  Google Scholar 

  14. Wardlaw JM, Smith EE, Biessels GJ, Cordonnier C, Fazekas F, Frayne R, Lindley RI, O'Brien JT, Barkhof F, Benavente OR, Black SE, Brayne C, Breteler M, Chabriat H, Decarli C, de Leeuw FE, Doubal F, Duering M, Fox NC, Greenberg S, Hachinski V, Kilimann I, Mok V, Oostenbrugge R, Pantoni L, Speck O, Stephan BC, Teipel S, Viswanathan A, Werring D, Chen C, Smith C, van Buchem M, Norrving B, Gorelick PB, Dichgans M, STandards for ReportIng Vascular changes on nEuroimaging (STRIVE v1) (2013) Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 12:822–838

    Article  PubMed  PubMed Central  Google Scholar 

  15. Stock KW, Wetzel S, Kirsch E, Bongartz G, Steinbrich W, Radue EW (1996) Anatomic evaluation of the circle of Willis: MR angiography versus intraarterial digital subtraction angiography. AJNR Am J Neuroradiol 17:1495–1499

    CAS  PubMed  Google Scholar 

  16. Samuels OB, Joseph GJ, Lynn MJ, Smith HA, Chimowitz MI (2000) A standardized method for measuring intracranial arterial stenosis. AJNR Am J Neuroradiol 21:643–646

    CAS  PubMed  Google Scholar 

  17. Krabbe-Hartkamp MJ, van der Grond J, de Leeuw FE, de Groot JC, Algra A, Hillen B, Breteler MM, Mali WP (1998) Circle of Willis: morphologic variation on three-dimensional time-off light MR angiograms. Radiology 207:103–111

    Article  CAS  PubMed  Google Scholar 

  18. Kapoor K, Singh B, Dewan LI (2008) Variations in the configuration of the circle of Willis. Anat Sci Int 83:96–106

    Article  PubMed  Google Scholar 

  19. Zaninovich OA, Ramey WL, Walter CM, Dumont TM (2017) Completion of the circle of Willis varies by gender, age, and indication for computed tomography angiography. World Neurosurg 106:953–963

    Article  PubMed  Google Scholar 

  20. Henderson RD, Eliasziw M, Fox AJ, Rothwell PM, Barnett HJ (2000) Angiographically defined collateral circulation and risk of stroke in patients with severe carotid artery stenosis. Stroke 31:128–132

    Article  CAS  PubMed  Google Scholar 

  21. Miyazawa N, Shinohara T, Yamagata Z (2011) Association of incompleteness of the anterior part of the circle of Willis with the occurrence of lacunes in the basal ganglia. Eur J Neurol 18:1358–1360

    Article  CAS  PubMed  Google Scholar 

  22. Chuang YM, Huang KL, Chang YJ, Chang CH, Chang TY, Wu TC, Lin CP, Wong HF, Liu SJ, Lee TH (2011) Associations between circle of Willis morphology and white matter lesion load in subjects with carotid artery stenosis. Eur Neurol 66:136–144

    Article  PubMed  Google Scholar 

  23. Saba L, Raz E, Fatterpekar G, Montisci R, di Martino M, Bassareo PP, Piga M (2015) Correlation between leukoaraiosis volume and circle of Willis variants. J Neuroimaging 25:226–231

    Article  PubMed  Google Scholar 

  24. Saba L, Sanfilippo R, Porcu M, Lucatelli P, Montisci R, Zaccagna F, Suri JS, Anzidei M, Wintermark M (2017) Relationship between white matter hyperintensities volume and the circle of Willis configurations in patients with carotid artery pathology. Eur J Radiol 89:111–116

    Article  PubMed  Google Scholar 

  25. Ren Y, Chen Q, Li ZY (2015) A 3D numerical study of the collateral capacity of the circle of Willis with anatomical variation in the posterior circulation. Biomed Eng Online 14:S11

    Article  PubMed  PubMed Central  Google Scholar 

  26. Ryan DJ, Byrne S, Dunne R, Harmon M, Harbison J (2015) White matter disease and an incomplete circle of Willis. Int J Stroke 10:547–552

    Article  PubMed  Google Scholar 

  27. Li H, Xiong Y, Xu G, Zhang R, Zhu W, Yin Q, Ma M, Fan X, Yang F, Liu W, Duan Z, Liu X (2015) The circle of Willis and white matter lesions in patients with carotid atherosclerosis. J Stroke Cerebrovasc Dis 24:1749–1754

    Article  PubMed  Google Scholar 

  28. Hartkamp MJ, van Der Grond J, van Everdingen KJ, Hillen B, Mali WP (1999) Circle of Willis collateral flow investigated by magnetic resonance angiography. Stroke 30:2671–2678

    Article  CAS  PubMed  Google Scholar 

  29. Hendrikse J, Eikelboom BC, van der Grond J (2002) Magnetic resonance angiography of collateral compensation in asymptomatic and symptomatic internal carotid artery stenosis. J Vasc Surg 36:799–805

    Article  PubMed  Google Scholar 

  30. Men X, Wu A, Zhang B, Li H, Zhang Z, Chen S, Lin Y, Lu Z (2013) Leukoaraiosis and NIHSS score help to differentiate subtypes of intracranial branch atheromatous disease in southern Han Chinese patients with stroke. Neurol Sci 34:1727–1733

    Article  PubMed  Google Scholar 

  31. Wardlaw JM, Allerhand M, Doubal FN, Valdes Hernandez M, Morris Z, Gow AJ, Bastin M, Starr JM, Dennis MS, Deary IJ (2014) Vascular risk factors, large-artery atheroma, and brain white matter hyperintensities. Neurology 82:1–8

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Cerebrovascular Disease Center, Department of Neurology, People’s Hospital, China Medical University, 33 Wenyi Road, Shenhe District, Shenyang, 110016, People’s Republic of China

    Huirong Ye, Xiumei Wu, Jiangzhi Yan, Jian Wang, Jianting Qiu & Yujie Wang

Authors
  1. Huirong Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiumei Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiangzhi Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jian Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jianting Qiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yujie Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yujie Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ye, H., Wu, X., Yan, J. et al. Completeness of circle of Willis and white matter hyperintensities in patients with severe internal carotid artery stenosis. Neurol Sci 40, 509–514 (2019). https://doi.org/10.1007/s10072-018-3683-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-018-3683-9

Keywords

Search

Navigation