Skip to main content

Advertisement

Log in

Silent brain infarcts and white matter lesions in patients with asymptomatic carotid stenosis

  • Original article
  • Published:
Acta Neurologica Belgica Aims and scope Submit manuscript

Abstract

The association of carotid atherosclerosis with silent brain infarcts (SBIs) and white matter lesions (WMLs) currently remains unknown. This study aims to compare SBIs, deep white matter lesions (DWMLs), and periventricular white matter lesions (PWMLs) in ipsilateral and contralateral hemispheres to internal carotid artery (ICA) stenosis, and investigate their association with stenosis grade in patients with asymptomatic ≥ 50% unilateral extracranial ICA stenosis. Patients without previous history of stroke and/or transient ischemic attack who had ≥ 50% stenosis in unilateral ICA on carotid color Doppler ultrasound were enrolled in the study. Patient demographics, vascular risk factors and ICA stenosis grades; number, location, and size of SBIs, DWMLs, and PWMLs in ICA territory were evaluated in both hemispheres using magnetic resonance imaging of the brain. Of the 69 patients, 53 had 50–69% (76.8%) and 16 had ≥ 70% (23.2%) unilateral ICA stenosis. There was no statistically significant difference in SBIs between ipsilateral and contralateral hemispheres to ≥ 50% ICA stenosis. Comparison of ICA stenoses as 50–69% and ≥ 70% revealed a greater number of patients with SBI in ipsilateral hemisphere to ≥ 70% stenosis compared to contralateral (p = 0.025). The number of SBIs was also higher in ipsilateral hemisphere to ≥ 70% stenosis compared to contralateral (p = 0.022). While DWMLs and PWMLs did not differ between hemispheres, frequency of Fazekas grade 1 DWMLs was lower in ipsilateral hemisphere to either 50–69% or ≥ 70% ICA stenosis compared to contralateral (p = 0.035 and p = 0.025, respectively). Results of the present study indicate that stenosis grade may be relevant in the association between asymptomatic carotid stenosis and SBIs, and ≥ 70% stenosis may pose a risk of SBI development.

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

Access this article

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. Fanning JP, Wesley AJ, Wong AA, Fraser JF (2014) Emerging spectra of silent brain infarction. Stroke 45:3461–3471. https://doi.org/10.1161/STROKEAHA.114.005919

    Article  PubMed  Google Scholar 

  2. Zhu YC, Dufouil C, Tzourio C, Chabriat H (2011) Silent brain infarcts: a review of MRI diagnostic criteria. Stroke 42:1140–1145. https://doi.org/10.1161/STROKEAHA.110.60011

    Article  PubMed  Google Scholar 

  3. Fisher CM (1965) Lacunes: small, deep cerebral infarcts. Neurology 15:774–784. https://doi.org/10.1212/wnl.15.8.774

    Article  PubMed  CAS  Google Scholar 

  4. Fanning JP, Wong AA, Fraser JF (2014) The epidemiology of silent brain infarction: a systematic review of population-based cohorts. BMC Med 12:119. https://doi.org/10.1186/s12916-014-0119-0

    Article  PubMed  PubMed Central  Google Scholar 

  5. Astarci P, Glineur D, Kefer J, D'Hoore W, Renkin J, Vanoverschelde JL, El Khoury G, Grandin C (2011) Magnetic resonance imaging evaluation of cerebral embolization during percutaneous aortic valve implantation: comparison of transfemoral and trans-apical approaches using Edwards Sapiens valve. Eur J CardiothoracSurg 40:475–479. https://doi.org/10.1016/j.ejcts.2010.11.070

    Article  Google Scholar 

  6. Bernick C, Kuller L, Dulberg C, Longstreth WT Jr, Manolio T, Beauchamp N, Price T, Cardiovascular Health Study Collaborative Reseach Group (2001) Silent MRI infarcts and the risk of future stroke: the cardiovascular health study. Neurology 57:1222–1229. https://doi.org/10.1212/wnl.57.7.1222

    Article  PubMed  CAS  Google Scholar 

  7. Bokura H, Kobayashi S, Yamaguchi S, Iijima K, Nagai A, Toyoda G, Oguro H, Takahashi K (2006) Silent brain infarction and subcortical white matter lesions increase the risk of stroke and mortality: a prospective cohort study. J Stroke Cerebrovasc Dis 15:57–63. https://doi.org/10.1016/j.jstrokecerebrovasdis.2005.11.001

    Article  PubMed  Google Scholar 

  8. 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. https://doi.org/10.1136/bmj.c3666

    Article  PubMed  PubMed Central  Google Scholar 

  9. Windham BG, Deere B, Griswold ME, Wang W, Bezerra DC, Shibata D, Butler K, Knopman D, Gottesman RF, Heiss G, Mosley TH Jr (2015) Small brain lesions and incident stroke and mortality: a cohort study. Ann Intern Med 163:22–31. https://doi.org/10.7326/M14-2057

    Article  PubMed  PubMed Central  Google Scholar 

  10. Prabhakaran S, Wright CB, Yoshita M, Delapaz R, Brown T, DeCarli C, Sacco RL (2008) Prevalence and determinants of subclinical brain infarction: the Northern Manhattan Study. Neurology 70:425–430. https://doi.org/10.1212/01.wnl.0000277521.66947.e5

    Article  PubMed  CAS  Google Scholar 

  11. Longstreth WT Jr, Bernick C, Manolio TA, Bryan N, Jungreis CA, Price TR (1998) Lacunar infarcts defined by magnetic resonance imaging of 3660 elderly people: the Cardiovascular Health Study. Arch Neurol 55:1217–1225. https://doi.org/10.1001/archneur.55.9.1217

    Article  PubMed  Google Scholar 

  12. Vermeer SE, Koudstaal PJ, Oudkerk M, Hofman A, Breteler MM (2002) Prevalence and risk factors of silent brain infarcts in the population-based Rotterdam Scan Study. Stroke 33:21–25. https://doi.org/10.1161/hs0102.101629

    Article  PubMed  Google Scholar 

  13. Howard G, Wagenknecht LE, Cai J, Cooper L, Kraut MA, Toole JF (1998) Cigarette smoking and other risk factors for silent cerebral infarction in the general population. Stroke 29:913–917. https://doi.org/10.1161/01.str.29.5.913

    Article  PubMed  CAS  Google Scholar 

  14. Price TR, Manolio TA, Kronmal RA, Kittner SJ, Yue NC, Robbins J, Anton-Culver H, O'Leary DH (1997) Silent brain infarction on magnetic resonance imaging and neurological abnormalities in community-dwelling older adults. The Cardiovascular Health Study. CHS Collaborative Research Group. Stroke 28:1158–1164. https://doi.org/10.1161/01.str.28.6.1158

    Article  PubMed  CAS  Google Scholar 

  15. Wright CB, Festa JR, Paik MC, Schmiedigen A, Brown TR, Yoshita M, DeCarli C, Sacco R, Stern Y (2008) White matter hyperintensities and subclinical infarction: associations with psychomotor speed and cognitive flexibility. Stroke 39:800–805. https://doi.org/10.1161/STROKEAHA.107.484147

    Article  PubMed  PubMed Central  Google Scholar 

  16. Avdibegović E, Bećirović E, Selimbasić Z, Hasanović M, Sinanović O (2007) Cerebral cortical atrophy and silent brain infarcts in psychiatric patients. PsychiatrDanub 19:49–55

    Google Scholar 

  17. Kobayashi S, Okada K, Koide H, Bokura H, Yamaguchi S (1997) Subcortical silent brain infarction as a risk factor for clinical stroke. Stroke 28:1932–1939. https://doi.org/10.1161/01.str.28.10.1932

    Article  PubMed  CAS  Google Scholar 

  18. Vermeer SE, Hollander M, van Dijk EJ, Hofman A, Koudstaal PJ, Breteler MM, Rotterdam Scan Study (2003) Silent brain infarcts and white matter lesions increase stroke risk in the general population: the Rotterdam Scan Study. Stroke 34:1126–1129. https://doi.org/10.1161/01.STR.0000068408.82115.D2

    Article  PubMed  Google Scholar 

  19. Gupta A, Giambrone AE, Gialdini G, Finn C, Delgado D, Gutierrez J, Wright C, Beiser AS, Seshadri S, Pandya A, Kamel H (2016) Silent brain infarction and risk of future stroke: a systematic review and meta-analysis. Stroke 47:719–725. https://doi.org/10.1161/STROKEAHA.115.011889

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Jayasooriya G, Thapar A, Shalhoub J, Davies AH (2011) Silent cerebral events in asymptomatic carotid stenosis. J VascSurg 54:227–236. https://doi.org/10.1016/j.jvs.2011.01.037

    Article  Google Scholar 

  21. Kim KW, MacFall JR, Payne ME (2008) Classification of white matter lesions on magnetic resonance imaging in elderly. Biol Psychiatry 64:273–280. https://doi.org/10.1016/j.biopsych.2008.03.024

    Article  PubMed  PubMed Central  Google Scholar 

  22. Baezner H, Blahak C, Poggesi A, Pantoni L, Inzitari D, Chabriat H, Erkinjuntti T, Fazekas F, Ferro JM, Langhorne P, O'Brien J, Scheltens P, Visser MC, Wahlund LO, Waldemar G, Wallin A, Hennerici MG, LADIS Study Group (2008) Association of gait and balance disorders with age-related white matter changes: the LADIS study. Neurology 70:935–942. https://doi.org/10.1212/01.wnl.0000305959.46197.e6

    Article  PubMed  CAS  Google Scholar 

  23. Gouw AA, Seewann A, van der Flier WM, Barkhof F, Rozemuller AM, Scheltens P, Geurts JJ (2011) Heterogeneity of small vessel disease: a systematic review of MRI and histopathology correlations. J NeurolNeurosurg Psychiatry 82:126–135. https://doi.org/10.1136/jnnp.2009.204685

    Article  Google Scholar 

  24. Grant EG, Benson CB, Moneta GL, Alexandrov AV, Baker JD, Bluth EI, Carroll BA, Eliasziw M, Gocke J, Hertzberg BS, Katanick S, Needleman L, Pellerito J, Polak JF, Rholl KS, Wooster DL, Zierler RE (2003) Carotid artery stenosis: gray-scale and Doppler US diagnosis—Society of Radiologists in Ultrasound Consensus Conference. Radiology 229:340–346. https://doi.org/10.1148/radiol.2292030516

    Article  PubMed  Google Scholar 

  25. Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA (1987) MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol 149:351–356. https://doi.org/10.2214/ajr.149.2.351

    Article  PubMed  CAS  Google Scholar 

  26. Finn C, Giambrone AE, Gialdini G, Delgado D, Baradaran H, Kamel H, Gupta A (2017) The association between carotid artery atherosclerosis and silent brain infarction: a systematic review and meta-analysis. J Stroke Cerebrovasc Dis 26:1594–1601. https://doi.org/10.1016/j.jstrokecerebrovasdis.2017.02.028

    Article  PubMed  PubMed Central  Google Scholar 

  27. Caplan LR, Hennerici M (1998) Impaired clearance of emboli (washout) is an important link between hypoperfusion, embolism, and ischemic stroke. Arch Neurol 55:1475–1482. https://doi.org/10.1001/archneur.55.11.1475

    Article  PubMed  CAS  Google Scholar 

  28. Kotani K, Osaki Y, Sakane N, Adachi S, Ishimaru Y (2004) Risk factors for silent cerebral infarction in the elderly. Arch Med Res 35:522–524. https://doi.org/10.1016/j.arcmed.2004.07.003

    Article  PubMed  Google Scholar 

  29. Uehara T, Tabuchi M, Mori E (1999) Risk factors for silent cerebral infarcts in subcortical white matter and basal ganglia. Stroke 30:378–382. https://doi.org/10.1161/01.str.30.2.378

    Article  PubMed  CAS  Google Scholar 

  30. Manolio TA, Burke GL, O'Leary DH, Evans G, Beauchamp N, Knepper L, Ward B (1999) Relationships of cerebral MRI findings to ultrasonographic carotid atherosclerosis in older adults: the Cardiovascular Health Study. CHS Collaborative Research Group. ArteriosclerThrombVascBiol 19:356–365. https://doi.org/10.1161/01.atv.19.2.356

    Article  CAS  Google Scholar 

  31. Baradaran H, Gialdini G, Mtui E, Askin G, Kamel H, Gupta A (2016) Silent brain infarction in patients with asymptomatic carotid artery atherosclerotic disease. Stroke 47:1368–1370. https://doi.org/10.1161/STROKEAHA.116.013193

    Article  PubMed  Google Scholar 

  32. Takahashi W, Fujii H, Ide M, Takagi S, Shinohara Y (2005) Atherosclerotic changes in intracranial and extracranial large arteries in apparently healthy persons with asymptomatic lacunar infarction. J Stroke Cerebrovasc Dis 14:17–22. https://doi.org/10.1016/j.jstrokecerebrovasdis.2004.10.003

    Article  PubMed  Google Scholar 

  33. Inoue K, Matsumoto M, Shono T, Toyokawa S, Moriki A (2007) Increased intima media thickness and atherosclerotic plaques in the carotid artery as risk factors for silent brain infarcts. J Stroke Cerebrovasc Dis 16:14–20. https://doi.org/10.1016/j.jstrokecerebrovasdis.2006.08.001

    Article  PubMed  Google Scholar 

  34. Pini R, Faggioli G, Longhi M, Vacirca A, Gallitto E, Freyrie A, Gargiulo M, Stella A (2016) The detrimental impact of silent cerebral infarcts on asymptomatic carotid endarterectomy outcome. J VascSurg 64:15–24. https://doi.org/10.1016/j.jvs.2015.12.049

    Article  Google Scholar 

  35. Moroni F, Ammirati E, Magnoni M, D'Ascenzo F, Anselmino M, Anzalone N, Rocca MA, Falini A, Filippi M, Camici PG (2016) Carotid atherosclerosis, silent ischemic brain damage and brain atrophy: a systematic review and meta-analysis. Int J Cardiol 223:681–687. https://doi.org/10.1016/j.ijcard.2016.08.234

    Article  PubMed  Google Scholar 

  36. Kwee RM, Hofman PA, Gronenschild EH, van Oostenbrugge RJ, Mess WH, ter Berg JW, Franke CL, Korten AG, Meems BJ, van Engelshoven JM, Wildberger JE, Kooi ME (2011) Association between carotid plaque characteristics and cerebral white matter lesions: one-year follow-up study by MRI. PLoS ONE 6:e17070. https://doi.org/10.1371/journal.pone.0017070

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Ammirati E, Moroni F, Magnoni M, Rocca MA, Messina R, Anzalone N, De Filippis C, Scotti I, Besana F, Spagnolo P, Rimoldi OE, Chiesa R, Falini A, Filippi M, Camici PG (2017) Relation between characteristics of carotid atherosclerotic plaques and brain white matter hyperintensities in asymptomatic patients. Sci Rep 7:10559. https://doi.org/10.1038/s41598-017-11216-x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Chen YF, Kuo YS, Wu WC, Tang SC, Jiang SF (2018) Association between leukoaraiosis and cerebral blood flow territory alteration in asymptomatic internal carotid artery stenosis. ClinRadiol 73:502.e9–502.e14. https://doi.org/10.1016/j.crad.2017.12.006

    Article  Google Scholar 

  39. de Leeuw FE, de Groot JC, Oudkerk M, Witteman JC, Hofman A, van Gijn J, Breteler MM (2002) Hypertension and cerebral white matter lesions in a prospective cohort study. Brain 125(Pt 4):765–772. https://doi.org/10.1093/brain/awf077

    Article  PubMed  Google Scholar 

  40. de Leeuw FE, de Groot JC, Achten E, Oudkerk M, Ramos LM, Heijboer R, Hofman A, Jolles J, van Gijn J, Breteler MM (2001) Prevalence of cerebral white matter lesions in elderly people: a population based magnetic resonance imaging study. The Rotterdam Scan Study. J NeurolNeurosurg Psychiatry 70:9–14. https://doi.org/10.1136/jnnp.70.1.9

    Article  Google Scholar 

  41. Kandiah N, Goh O, Mak E, Marmin M, Ng A (2014) Carotid stenosis: a risk factor for cerebral white-matter disease. J Stroke Cerebrovasc Dis 23:136–139. https://doi.org/10.1016/j.jstrokecerebrovasdis.2012.11.007

    Article  PubMed  Google Scholar 

  42. Bots ML, van Swieten JC, Breteler MM, de Jong PT, van Gijn J, Hofman A, Grobbee DE (1993) Cerebral white matter lesions and atherosclerosis in the Rotterdam Study. Lancet 341:1232–1237. https://doi.org/10.1016/0140-6736(93)91144-b

    Article  PubMed  CAS  Google Scholar 

  43. Brisset M, Boutouyrie P, Pico F, Zhu Y, Zureik M, Schilling S, Dufouil C, Mazoyer B, Laurent S, Tzourio C, Debette S (2013) Large-vessel correlates of cerebral small-vessel disease. Neurology 80:662–669. https://doi.org/10.1212/WNL.0b013e318281ccc2

    Article  PubMed  PubMed Central  Google Scholar 

  44. Saba L, Sanfilippo R, Pascalis L, Montisci R, Mallarini G (2009) Carotid artery abnormalities and leukoaraiosis in elderly patients: evaluation with MDCT. AJR Am J Roentgenol 192:W63–70. https://doi.org/10.2214/AJR.07.3566

    Article  PubMed  Google Scholar 

  45. Potter GM, Doubal FN, Jackson CA, Sudlow CL, Dennis MS, Wardlaw JM (2012) Lack of association of white matter lesions with ipsilateral carotid artery stenosis. Cerebrovasc Dis 33:378–384. https://doi.org/10.1159/000336762

    Article  PubMed  PubMed Central  Google Scholar 

  46. Adachi T, Takagi M, Hoshino H, Inafuku T (1997) Effect of extracranial carotid artery stenosis and other risk factors for stroke on periventricular hyperintensity. Stroke 28:2174–2179. https://doi.org/10.1161/01.str.28.11.2174

    Article  PubMed  CAS  Google Scholar 

  47. 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. https://doi.org/10.1136/bmjopen-2017-020830

    Article  PubMed  PubMed Central  Google Scholar 

  48. Baradaran H, Mtui EE, Richardson JE, Delgado D, Gupta A (2017) Hemispheric differences in leukoaraiosis in patients with carotid artery stenosis: a systematic review. ClinNeuroradiol 27:7–13. https://doi.org/10.1007/s00062-015-0402-2

    Article  CAS  Google Scholar 

  49. ThusharaVijayakumar N, Sangwan A, Sharma B, Majid A, Rajanikant GK (2016) Cerebral ischemic preconditioning: the road so far…. MolNeurobiol 53:2579–2593. https://doi.org/10.1007/s12035-015-9278-z

    Article  CAS  Google Scholar 

  50. Thompson JW, Dave KR, Young JI, Perez-Pinzon MA (2013) Ischemic preconditioning alters the epigenetic profile of the brain from ischemic intolerance to ischemic tolerance. Neurotherapeutics 10:789–797. https://doi.org/10.1007/s13311-013-0202-9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Chaturvedi S, Sacco RL (2015) How recent data have impacted the treatment of internal carotid artery stenosis. J Am CollCardiol 65:1134–1143. https://doi.org/10.1016/j.jacc.2014.12.045

    Article  Google Scholar 

  52. Dharmakidari S, Bhattacharya P, Chaturvedi S (2017) Carotid artery stenosis: medical therapy, surgery, and stenting. CurrNeurolNeurosci Rep 17:77. https://doi.org/10.1007/s11910-017-0786-2

    Article  Google Scholar 

  53. Salem MM, Alturki AY, Fusco MR, Thomas AJ, Carter BS, Chen CC, Kasper EM (2018) Carotid artery stenting vs. carotid endarterectomy in the management of carotid artery stenosis: lessons learned from randomized controlled trials. SurgNeurolInt 9:85. https://doi.org/10.4103/sni.sni_400_17

    Article  Google Scholar 

  54. Paraskevas KI, Veith FJ, Spence JD (2018) How to identify which patients with asymptomatic carotid stenosis could benefit from endarterectomy or stenting. Stroke VascNeurol 3:92–100. https://doi.org/10.1136/svn-2017-000129

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bülent Güven.

Ethics declarations

Conflict of interest

The authors report no conflicts of interest.

Ethics approval

The study was carried out according to the Helsinki Declaration and was approved by the Institutional Ethics Committee.

Informed consent

All patients participating in the study provided written informed consent.

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

Benli, M.D., Güven, B., Güven, H. et al. Silent brain infarcts and white matter lesions in patients with asymptomatic carotid stenosis. Acta Neurol Belg 121, 983–991 (2021). https://doi.org/10.1007/s13760-020-01517-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13760-020-01517-w

Keywords

Navigation