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Risk factors for silent new ischemic cerebral lesions following carotid artery stenting

  • Interventional Neuroradiology
  • Published:
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Abstract

Purpose

Silent new ischemic cerebral lesions (sNICL) detected by diffusion-weighted imaging (DWI) are common after carotid artery stenting (CAS). As part of the Revascularization of Extracranial Carotid Artery Stenosis (RECAS) study, this work aimed to determine predictors of sNICL detected by DWI following CAS.

Methods

A total of 694 patients eligible for the RECAS study treated in Xuanwu Hospital, Capital Medical University, with complete imaging data were included in this retrospective study. The patients were asymptomatic after CAS, and those with stroke, transient ischemic attack (TIA), or death were excluded. The RECAS protocol specified that DWI was completed 1–7 days before the procedure and within 3 days after CAS. Several parameters were assessed for associations with sNICL occurrence after CAS in univariate analysis. Finally, multivariate analysis was performed to determine risk factors for sNICL.

Results

The rate of post-procedural sNICL in CAS was 51.3% (356/694 patients with sNICL). All patients underwent stenting with embolic protection devices. Univariate analysis showed that diabetes mellitus (P = 0.008), ipsilateral calcified plaques (P = 0.036), ipsilateral ulcerated plaques (P = 0.026), pre-dilatation (P = 0.003), and open-cell stent use (P < 0.001) were significantly associated with sNICL occurrence in CAS. Multivariate analysis revealed that diabetes mellitus (P = 0.006), ipsilateral calcified plaques (P = 0.024), ipsilateral ulcerated plaques (P = 0.021), and open-cell stent use (P < 0.001) were independent risk factors for sNICL.

Conclusions

Patients with diabetes, calcified or ulcerated plaques who undergo CAS with open-cell stent application, are at high risk of sNICL. Large-scale prospective randomized controlled trials are needed to confirm these findings.

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Abbreviations

sNICL:

silent new ischemic cerebral lesions

DWI:

diffusion-weighted imaging

MRI:

magnetic resonance imaging

CAS:

carotid artery stenting

RECAS:

Revascularization of Extracranial Carotid Artery Stenosis

TIA:

transient ischemic attack

CEA:

carotid endarterectomy

ICA:

internal carotid artery

CTA:

computed tomography angiography

DSA:

digital subtraction angiography

MI:

myocardial infarction

DM:

diabetes mellitus

NASCET:

North American Symptomatic Carotid Endarterectomy Trial

AF:

atrial fibrillation

CCA:

common carotid arteries

EPD:

embolic protection device

SD:

standard deviation

OR:

odds ratio

CI:

confidence interval

References

  1. Bonati LH, Jongen LM, Haller S, Flach HZ, Dobson J, Nederkoorn PJ, Macdonald S, Gaines PA, Waaijer A, Stierli P, Jager HR, Lyrer PA, Kappelle LJ, Wetzel SG, van der Lugt A, Mali WP, Brown MM, van der Worp HB, Engelter ST (2010) New ischaemic brain lesions on MRI after stenting or endarterectomy for symptomatic carotid stenosis: a substudy of the International Carotid Stenting Study (ICSS). Lancet Neurol 9(4):353–362. https://doi.org/10.1016/s1474-4422(10)70057-0

    Article  PubMed  Google Scholar 

  2. Ishii D, Sakamoto S, Okazaki T, Matsushige T, Shinagawa K, Ichinose N, Kurisu K (2018) Overlapped stenting is associated with postoperative hypotension after carotid artery stenting. J Stroke Cerebrovasc Dis 27(3):653–659. https://doi.org/10.1016/j.jstrokecerebrovasdis.2017.09.041

    Article  PubMed  Google Scholar 

  3. Bendszus M, Stoll G (2006) Silent cerebral ischaemia: hidden fingerprints of invasive medical procedures. Lancet Neurol 5(4):364–372. https://doi.org/10.1016/s1474-4422(06)70412-4

    Article  PubMed  Google Scholar 

  4. Cosottini M, Michelassi MC, Puglioli M, Lazzarotti G, Orlandi G, Marconi F, Parenti G, Bartolozzi C (2005) Silent cerebral ischemia detected with diffusion-weighted imaging in patients treated with protected and unprotected carotid artery stenting. Stroke 36(11):2389–2393. https://doi.org/10.1161/01.STR.0000185676.05358.f2

    Article  PubMed  Google Scholar 

  5. Yadav JS, Roubin GS, Iyer S, Vitek J, King P, Jordan WD, Fisher WS (1997) Elective stenting of the extracranial carotid arteries. Circulation 95(2):376–381. https://doi.org/10.1161/01.cir.95.2.376

    Article  CAS  PubMed  Google Scholar 

  6. Lin C, Tang X, Shi Z, Zhang L, Yan D, Niu C, Zhou M, Wang L, Fu W, Guo D (2018) Serum tumor necrosis factor alpha levels are associated with new ischemic brain lesions after carotid artery stenting. J Vasc Surg 68(3):771–778. https://doi.org/10.1016/j.jvs.2017.11.085

    Article  PubMed  Google Scholar 

  7. Maggio P, Altamura C, Lupoi D, Paolucci M, Altavilla R, Tibuzzi F, Passarelli F, Arpesani R, Di Giambattista G, Grasso RF, Luppi G, Fiacco F, Silvestrini M, Pasqualetti P, Vernieri F (2017) The role of white matter damage in the risk of periprocedural diffusion-weighted lesions after carotid artery stenting. Cerebrovasc Dis Extra 7(1):1–8. https://doi.org/10.1159/000452717

    Article  PubMed  PubMed Central  Google Scholar 

  8. Kashiwazaki D, Kuwayama N, Akioka N, Noguchi K, Kuroda S (2017) Carotid plaque with expansive arterial remodeling is a risk factor for ischemic complication following carotid artery stenting. Acta Neurochir 159(7):1299–1304. https://doi.org/10.1007/s00701-017-3188-y

    Article  PubMed  Google Scholar 

  9. Kuliha M, Roubec M, Goldírová A, Hurtíková E, Jonszta T, Procházka V, Gumulec J, Herzig R, Školoudík D (2016) Laboratory-based markers as predictors of brain infarction during carotid stenting: a prospective study. J Atheroscler Thromb 23(7):839–847. https://doi.org/10.5551/jat.31799

    Article  CAS  PubMed  Google Scholar 

  10. Koyanagi M, Yoshida K, Kurosaki Y, Sadamasa N, Narumi O, Sato T, Chin M, Handa A, Yamagata S, Miyamoto S (2016) Reduced cerebrovascular reserve is associated with an increased risk of postoperative ischemic lesions during carotid artery stenting. J Neurointervention Surg 8(6):576–580. https://doi.org/10.1136/neurintsurg-2014-011163

    Article  Google Scholar 

  11. Pendlebury ST, Rothwell PM (2009) Prevalence, incidence, and factors associated with pre-stroke and post-stroke dementia: a systematic review and meta-analysis. Lancet Neurol 8(11):1006–1018. https://doi.org/10.1016/s1474-4422(09)70236-4

    Article  PubMed  Google Scholar 

  12. Gensicke H, van der Worp HB, Nederkoorn PJ, Macdonald S, Gaines PA, van der Lugt A, Mali WP, Lyrer PA, Peters N, Featherstone RL, de Borst GJ, Engelter ST, Brown MM, Bonati LH (2015) Ischemic brain lesions after carotid artery stenting increase future cerebrovascular risk. J Am Coll Cardiol 65(6):521–529. https://doi.org/10.1016/j.jacc.2014.11.038

    Article  PubMed  PubMed Central  Google Scholar 

  13. Poppert H, Wolf O, Theiss W, Heider P, Hollweck R, Roettinger M, Sander D (2006) MRI lesions after invasive therapy of carotid artery stenosis: a risk-modeling analysis. Neurol Res 28(5):563–567. https://doi.org/10.1179/016164105X49391

    Article  CAS  PubMed  Google Scholar 

  14. Barnett HJM, Taylor DW, Haynes RB, Sackett DL, Peerless SJ, Ferguson GG, Fox AJ, Rankin RN, Hachinski VC, Wiebers DO, Eliasziw M (1991) Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med 325(7):445–453. https://doi.org/10.1056/nejm199108153250701

    Article  CAS  PubMed  Google Scholar 

  15. Russjan A, Goebell E, Havemeister S, Thomalla G, Cheng B, Beck C, Krützelmann A, Fiehler J, Gerloff C, Rosenkranz M (2012) Predictors of periprocedural brain lesions associated with carotid stenting. Cerebrovasc Dis (Basel, Switzerland) 33(1):30–36

    Article  Google Scholar 

  16. Jiao LQ, Song G, Li SM, Miao ZR, Zhu FS, Ji XM, Yin GY, Chen YF, Wang YB, Ma Y, Ling F (2013) Thirty-day outcome of carotid artery stenting in Chinese patients: a single-center experience. Chin Med J 126(20):3915–3920

    PubMed  Google Scholar 

  17. Simonsen CZ, Madsen MH, Schmitz ML, Mikkelsen IK, Fisher M, Andersen G (2015) Sensitivity of diffusion- and perfusion-weighted imaging for diagnosing acute ischemic stroke is 97.5%. Stroke 46(1):98–101. https://doi.org/10.1161/strokeaha.114.007107

    Article  PubMed  Google Scholar 

  18. Chung GH, Jeong JY, Kwak HS, Hwang SB (2016) Associations between cerebral embolism and carotid intraplaque hemorrhage during protected carotid artery stenting. AJNR Am J Neuroradiol 37(4):686–691. https://doi.org/10.3174/ajnr.A4576

    Article  CAS  PubMed  Google Scholar 

  19. Henry RMA, Kostense PJ, Dekker JM, Nijpels G, Heine RJ, Kamp O, Bouter LM, Stehouwer CDA (2004) Carotid arterial remodeling: a maladaptive phenomenon in type 2 diabetes but not in impaired glucose metabolism: the Hoorn study. Stroke 35(3):671–676

    Article  Google Scholar 

  20. Ikeda G, Tsuruta W, Nakai Y, Shiigai M, Marushima A, Masumoto T, Tsurushima H, Matsumura A (2014) Anatomical risk factors for ischemic lesions associated with carotid artery stenting. Interv Neuroradiol 20(6):746–754. https://doi.org/10.15274/inr-2014-10075

    Article  PubMed  PubMed Central  Google Scholar 

  21. Wimmer NJ, Yeh RW, Cutlip DE, Mauri L (2012) Risk prediction for adverse events after carotid artery stenting in higher surgical risk patients. Stroke 43(12):3218–3224

    Article  Google Scholar 

  22. Doig D, Hobson BM, Müller M, Jäger HR, Featherstone RL, Brown MM, Bonati LH, Richards T, Investigators I-MS (2016) Carotid anatomy does not predict the risk of new ischaemic brain lesions on diffusion-weighted imaging after carotid artery stenting in the ICSS-MRI substudy. Eur J Vasc Endovasc Surg 51(1):14–20

    Article  CAS  Google Scholar 

  23. Ichinose N, Hama S, Tsuji T, Soh Z, Hayashi H, Kiura Y, Sakamoto S, Okazaki T, Ishii D, Shinagawa K, Kurisu K (2018) Predicting ischemic stroke after carotid artery stenting based on proximal calcification and the jellyfish sign. J Neurosurg 128(5):1280–1288. https://doi.org/10.3171/2017.1.jns162379

    Article  CAS  PubMed  Google Scholar 

  24. Wodarg F, Turner EL, Dobson J, Ringleb PA, Mali WP, Fraedrich G, Chatellier G, Bequemin JP, Brown MM, Algra A, Mas JL, Jansen O, Bonati LH (2018) Influence of stent design and use of protection devices on outcome of carotid artery stenting: a pooled analysis of individual patient data. J Neurointervention Surg 10(12):1149–1154. https://doi.org/10.1136/neurintsurg-2017-013622

    Article  Google Scholar 

  25. de Vries EE, Meershoek AJA, Vonken EJ, den Ruijter HM, van den Berg JC, de Borst GJ, Group ES (2019) A meta-analysis of the effect of stent design on clinical and radiologic outcomes of carotid artery stenting. J Vasc Surg 69(6):1952–1961 e1951. https://doi.org/10.1016/j.jvs.2018.11.017

    Article  PubMed  Google Scholar 

  26. Khan M, Qureshi AI (2014) Factors associated with increased rates of post-procedural stroke or death following carotid artery stent placement: a systematic review. J Vascular Intervention Neurol 7(1):11–20

    Google Scholar 

  27. Park KY, Chung PW, Kim YB, Moon HS, Suh BC, Yoon WT (2011) Post-interventional microembolism: cortical border zone is a preferential site for ischemia. Cerebrovasc Dis (Basel, Switzerland) 32(3):269–275

    Article  CAS  Google Scholar 

  28. Zhou W, Baughman BD, Soman S, Wintermark M, Lazzeroni LC, Hitchner E, Bhat J, Rosen A (2017) Volume of subclinical embolic infarct correlates to long-term cognitive changes after carotid revascularization. J Vasc Surg 65(3):686–694. https://doi.org/10.1016/j.jvs.2016.09.057

    Article  PubMed  Google Scholar 

  29. Gupta A, Baradaran H, Schweitzer AD, Kamel H, Pandya A, Delgado D, Dunning A, Mushlin AI, Sanelli PC (2013) Carotid plaque MRI and stroke risk: a systematic review and meta-analysis. Stroke 44(11):3071–3077

    Article  Google Scholar 

  30. Brinjikji W, Lehman VT, Huston J, Murad MH, Lanzino G, Cloft HJ, Kallmes DF (2017) The association between carotid intraplaque hemorrhage and outcomes of carotid stenting: a systematic review and meta-analysis. J Neurointervention Surg 9(9):837–842. https://doi.org/10.1136/neurintsurg-2016-012593

    Article  Google Scholar 

  31. Muller MD, Ahlhelm FJ, von Hessling A, Doig D, Nederkoorn PJ, Macdonald S, Lyrer PA, van der Lugt A, Hendrikse J, Stippich C, van der Worp HB, Richards T, Brown MM, Engelter ST, Bonati LH (2017) Vascular anatomy predicts the risk of cerebral ischemia in patients randomized to carotid stenting versus endarterectomy. Stroke 48(5):1285–1292. https://doi.org/10.1161/strokeaha.116.014612

    Article  PubMed  Google Scholar 

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Acknowledgements

None.

Funding

This study was funded by the National Key Research and Development Program of China (2016YFC1301703) and Beijing Science and Technology Commission (D161100003816002).

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Author notes

  1. Xiaoyu Xu and Yao Feng contributed equally to this work.

Authors and Affiliations

  1. Interventional Radiology Diagnosis and Treatment Center, Department of Neurosurgery, Xuanwu Hospital, Capital Medical University, Beijing, China

    Xiaoyu Xu, Yao Feng, Xuesong Bai, Yan Ma, Yabing Wang, Yanfei Chen, Bin Yang, Feng Ling & Liqun Jiao

  2. Department of Neurology, 1st People’s Hospital of Zhengzhou, Zhengzhou, China

    Xiaoyu Xu & Xiaoman Zhang

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  1. Xiaoyu Xu
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Correspondence to Liqun Jiao.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and national research committee (Ethics committees of the Xuanwu Hospital Capital Medical University) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Xu, X., Feng, Y., Bai, X. et al. Risk factors for silent new ischemic cerebral lesions following carotid artery stenting. Neuroradiology 62, 1177–1184 (2020). https://doi.org/10.1007/s00234-020-02447-3

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