Multiple predictors of in-stent restenosis after stent implantation in symptomatic intracranial atherosclerotic stenosis

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  • 1 Departments of Interventional Neuroradiology and
  • | 2 Neurology, Beijing Tiantan Hospital, Capital Medical University;
  • | 3 China National Clinical Research Center for Neurological Diseases;
  • | 4 Department of Cardiology, Beijing Anzhen Hospital, Capital Medical University, Beijing Institute of Heart Lung and Blood Vessel Diseases; and
  • | 5 Department of Radiology, Chinese People’s Liberation Army General Hospital, Beijing, China
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OBJECTIVE

This study aimed to identify predictors of intracranial in-stent restenosis (ISR) after stent placement in symptomatic intracranial atherosclerotic stenosis (ICAS).

METHODS

The authors retrospectively collected data from consecutive patients who suffered from symptomatic ICAS and underwent successful stent placement in Beijing Tiantan hospital. Eligible patients were classified into “ISR,” “indeterminate ISR,” or “no-ISR” groups by follow-up digital subtraction angiography or CT angiography. A multivariate logistic regression model was used to explore the predictors of intracranial ISR after adjustments for age and sex. In addition, ISR and no-ISR patients were divided into two groups based on the strongest predictor, and the incidence of ISR, recurrent stroke, and symptomatic ISR was compared between the two groups.

RESULTS

A total of 511 eligible patients were included in the study: 80 ISR, 232 indeterminate ISR, and 199 no-ISR patients. Elevated high-sensitivity C-reactive protein (hs-CRP; odds ratio [OR] 4.747, 95% confidence interval [CI] 2.253–10.01, p < 0.001), Mori type B and C (Mori type B vs Mori type A, OR 3.119, 95% CI 1.093–8.896, p = 0.033; Mori type C vs Mori type A, OR 4.780, 95% CI 1.244–18.37, p = 0.023), coronary artery disease (CAD; OR 2.721, 95% CI 1.192–6.212, p = 0.017), neutrophil/lymphocyte ratio (NLR; OR 1.474 95% CI 1.064–2.042, p = 0.020), residual stenosis (OR 1.050, 95% CI 1.022–1.080, p = 0.001) and concurrent intracranial tandem stenosis (OR 2.276, 95% CI 1.039–4.986, p = 0.040) synergistically contributed to the occurrence of intracranial ISR. Elevated hs-CRP (hs-CRP ≥ 3 mg/L) was the strongest predictor for ISR, and the incidence of ISR in the elevated hs-CRP group and normal hs-CRP group (hs-CRP < 3 mg/L) was 57.14% versus 21.52%, respectively, with recurrent stroke 44.64% versus 16.59%, and symptomatic ISR 41.07% versus 8.52%.

CONCLUSIONS

Elevated hs-CRP level, NLR, residual stenosis, Mori type B and C, CAD, and concurrent intracranial tandem stenosis are the main predictors of intracranial ISR, and elevated hs-CRP is crucially associated with recurrent stroke in patients with symptomatic ICAS after intracranial stent implantation.

ABBREVIATIONS

BA = basilar artery; BMS = bare-metal stent; CAD = coronary artery disease; CI = confidence interval; CTA = CT angiography; DAPT = dual antiplatelet therapy; DES = drug-eluting stent; DSA = digital subtraction angiography; ESR = erythrocyte sedimentation rate; hs-CRP = high-sensitivity C-reactive protein; ICA = internal carotid artery; ICAS = intracranial atherosclerotic stenosis; ISR = in-stent restenosis; LDL = low-density lipoprotein; MCA = middle cerebral artery; mRS = modified Rankin Scale; NIHSS = National Institutes of Health Stroke Scale; NLR = neutrophil/lymphocyte ratio; OR = odds ratio; PLR = platelet/lymphocyte ratio; TIA = transient ischemic attack; VA = vertebral artery; WEAVE = Wingspan Stent System Post Market Surveillance; WOVEN = Wingspan One-year Vascular Events and Neurologic Outcomes.

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  • 1

    Banerjee C, Chimowitz MI. Stroke caused by atherosclerosis of the major intracranial arteries. Circ Res. 2017;120(3):502513.

  • 2

    Zhou M, Wang H, Zeng X, Yin P, Zhu J, Chen W, et al. Mortality, morbidity, and risk factors in China and its provinces, 1990-2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet. 2019;394(10204):11451158.

    • Search Google Scholar
    • Export Citation
  • 3

    Alexander MJ, Zauner A, Chaloupka JC, Baxter B, Callison RC, Gupta R, et al. WEAVE trial: final results in 152 on-label patients. Stroke. 2019;50(4):889894.

    • Search Google Scholar
    • Export Citation
  • 4

    Alexander MJ, Zauner A, Gupta R, Alshekhlee A, Fraser JF, Toth G, et al. The WOVEN trial: Wingspan One-year Vascular Events and Neurologic Outcomes. J Neurointerv Surg. 2020;13(4):307310.

    • Search Google Scholar
    • Export Citation
  • 5

    Derdeyn CP, Fiorella D, Lynn MJ, Turan TN, Cotsonis GA, Lane BF, et al. Nonprocedural symptomatic infarction and in-stent restenosis after intracranial angioplasty and stenting in the SAMMPRIS trial (Stenting and Aggressive Medical Management for the Prevention of Recurrent Stroke in Intracranial Stenosis). Stroke. 2017;48(6):15011506.

    • Search Google Scholar
    • Export Citation
  • 6

    Fiorella DJ, Turk AS, Levy EI, Pride GL Jr, Woo HH, Albuquerque FC, et al. U.S. Wingspan Registry: 12-month follow-up results. Stroke. 2011;42(7):19761981.

    • Search Google Scholar
    • Export Citation
  • 7

    Turk AS, Levy EI, Albuquerque FC, Pride GL Jr, Woo H, Welch BG, et al. Influence of patient age and stenosis location on wingspan in-stent restenosis. AJNR Am J Neuroradiol. 2008;29(1):2327.

    • Search Google Scholar
    • Export Citation
  • 8

    Yu J, Wang L, Deng JP, Gao L, Zhang T, Zhao ZW, Gao GD. Treatment of symptomatic intracranial atherosclerotic stenosis with a normal-sized Gateway(™) balloon and Wingspan(™) stent. J Int Med Res. 2010;38(6):19681974.

    • Search Google Scholar
    • Export Citation
  • 9

    Kornowski R, Hong MK, Tio FO, Bramwell O, Wu H, Leon MB. In-stent restenosis: contributions of inflammatory responses and arterial injury to neointimal hyperplasia. J Am Coll Cardiol. 1998;31(1):224230.

    • Search Google Scholar
    • Export Citation
  • 10

    Fortmann SP, Ford E, Criqui MH, Folsom AR, Harris TB, Hong Y, et al. CDC/AHA Workshop on Markers of Inflammation and Cardiovascular Disease: Application to Clinical and Public Health Practice: report from the population science discussion group. Circulation. 2004;110(25):e554e559.

    • Search Google Scholar
    • Export Citation
  • 11

    Guo X, Ma N, Gao F, Mo DP, Luo G, Miao ZR. Corrigendum: Long-term risk factors for intracranial in-stent restenosis from a multicenter trial of stenting for symptomatic intracranial artery stenosis registry in China. Front Neurol. 2021;12:673264.

    • Search Google Scholar
    • Export Citation
  • 12

    Chimowitz MI, Lynn MJ, Howlett-Smith H, Stern BJ, Hertzberg VS, Frankel MR, et al. Comparison of warfarin and aspirin for symptomatic intracranial arterial stenosis. N Engl J Med. 2005;352(13):13051316.

    • Search Google Scholar
    • Export Citation
  • 13

    Mori T, Mori K, Fukuoka M, Arisawa M, Honda S. Percutaneous transluminal cerebral angioplasty: serial angiographic follow-up after successful dilatation. Neuroradiology. 1997;39(2):111116.

    • Search Google Scholar
    • Export Citation
  • 14

    Krischek O, Miloslavski E, Fischer S, Shrivastava S, Henkes H. A comparison of functional and physical properties of self-expanding intracranial stents [Neuroform3,. Wingspan, Solitaire, Leo+, Enterprise].Minim Invasive Neurosurg.2011;54(1):2128.

    • Search Google Scholar
    • Export Citation
  • 15

    Yue X, Xi G, Lu T, Xu G, Liu W, Zhang R, et al. Influence of residual stenosis on clinical outcome and restenosis after middle cerebral artery stenting. Cardiovasc Intervent Radiol. 2011;34(4):744750.

    • Search Google Scholar
    • Export Citation
  • 16

    Peng G, Zhang Y, Miao Z. Incidence and risk factors of in-stent restenosis for symptomatic intracranial atherosclerotic stenosis: a systematic review and meta-analysis. AJNR Am J Neuroradiol. 2020;41(8):14471452.

    • Search Google Scholar
    • Export Citation
  • 17

    Kang K, Zhang Y, Shuai J, Jiang C, Zhu Q, Chen K, et al. Balloon-mounted stenting for ICAS in a multicenter registry study in China: a comparison with the WEAVE/WOVEN trial. J Neurointerv Surg. Published online December 11, 2020.doi:10.1136/neurintsurg-2020-016658

    • Search Google Scholar
    • Export Citation
  • 18

    Falk E. Pathogenesis of atherosclerosis. J Am Coll Cardiol. 2006;47(8 suppl):C7C12.

  • 19

    Bhatt DL, Steg PG, Ohman EM, Hirsch AT, Ikeda Y, Mas JL, et al. International prevalence, recognition, and treatment of cardiovascular risk factors in outpatients with atherothrombosis. JAMA. 2006;295(2):180189.

    • Search Google Scholar
    • Export Citation
  • 20

    Ross R. Atherosclerosis—an inflammatory disease. N Engl J Med. 1999;340(2):115126.

  • 21

    Kibos A, Campeanu A, Tintoiu I. Pathophysiology of coronary artery in-stent restenosis. Acute Card Care. 2007;9(2):111119.

  • 22

    Farb A, Weber DK, Kolodgie FD, Burke AP, Virmani R. Morphological predictors of restenosis after coronary stenting in humans. Circulation. 2002;105(25):29742980.

    • Search Google Scholar
    • Export Citation
  • 23

    Lee MS, David EM, Makkar RR, Wilentz JR. Molecular and cellular basis of restenosis after percutaneous coronary intervention: the intertwining roles of platelets, leukocytes, and the coagulation-fibrinolysis system. J Pathol. 2004;203(4):861870.

    • Search Google Scholar
    • Export Citation
  • 24

    Gabay C, Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med. 1999;340(6):448454.

  • 25

    Weerasinghe D, McHugh KP, Ross FP, Brown EJ, Gisler RH, Imhof BA. A role for the alphavbeta3 integrin in the transmigration of monocytes. J Cell Biol. 1998;142(2):595607.

    • Search Google Scholar
    • Export Citation
  • 26

    Jukema JW, Verschuren JJW, Ahmed TAN, Quax PHA. Restenosis after PCI. Part 1: pathophysiology and risk factors. Nat Rev Cardiol. 2011;9(1):5362.

    • Search Google Scholar
    • Export Citation
  • 27

    Exner M, Schillinger M, Minar E, Mlekusch W, Schlerka G, Haumer M, et al. Heme oxygenase-1 gene promoter microsatellite polymorphism is associated with restenosis after percutaneous transluminal angioplasty. J Endovasc Ther. 2001;8(5):433440.

    • Search Google Scholar
    • Export Citation
  • 28

    Kumar A, Hoover JL, Simmons CA, Lindner V, Shebuski RJ. Remodeling and neointimal formation in the carotid artery of normal and P-selectin-deficient mice. Circulation. 1997;96(12):43334342.

    • Search Google Scholar
    • Export Citation
  • 29

    Cermak J, Key NS, Bach RR, Balla J, Jacob HS, Vercellotti GM. C-reactive protein induces human peripheral blood monocytes to synthesize tissue factor. Blood. 1993;82(2):513520.

    • Search Google Scholar
    • Export Citation
  • 30

    Buffon A, Liuzzo G, Biasucci LM, Pasqualetti P, Ramazzotti V, Rebuzzi AG, et al. Preprocedural serum levels of C-reactive protein predict early complications and late restenosis after coronary angioplasty. J Am Coll Cardiol. 1999;34(5):15121521.

    • Search Google Scholar
    • Export Citation
  • 31

    Niccoli G, Montone RA, Ferrante G, Crea F. The evolving role of inflammatory biomarkers in risk assessment after stent implantation. J Am Coll Cardiol. 2010;56(22):17831793.

    • Search Google Scholar
    • Export Citation
  • 32

    Gaspardone A, Versaci F, Tomai F, Citone C, Proietti I, Gioffrè G, Skossyreva O. C-Reactive protein, clinical outcome, and restenosis rates after implantation of different drug-eluting stents. Am J Cardiol. 2006;97(9):13111316.

    • Search Google Scholar
    • Export Citation
  • 33

    Higo T, Ueda Y, Oyabu J, Okada K, Nishio M, Hirata A, et al. Atherosclerotic and thrombogenic neointima formed over sirolimus drug-eluting stent: an angioscopic study. JACC Cardiovasc Imaging. 2009;2(5):616624.

    • Search Google Scholar
    • Export Citation
  • 34

    Gupta R, Bhatt A, Kassab M, Majid A. Elevated levels of pre-procedural high-sensitivity C-reactive protein is associated with midterm restenosis after extra- and intracranial stenting. J Neuroimaging. 2010;20(1):7477.

    • Search Google Scholar
    • Export Citation
  • 35

    Wang Z, Liu C, Fang H. Blood cell parameters and predicting coronary in-stent restenosis. Angiology. 2019;70(8):711718.

  • 36

    Li J, Zhao X, Meng X, Lin J, Liu L, Wang C, et al. High-sensitive C-reactive protein predicts recurrent stroke and poor functional outcome: subanalysis of the clopidogrel in high-risk patients with acute nondisabling cerebrovascular events trial. Stroke. 2016;47(8):20252030.

    • Search Google Scholar
    • Export Citation
  • 37

    Li J, Wang A, Zhao X, Liu L, Meng X, Lin J, et al. High-sensitive C-reactive protein and dual antiplatelet in intracranial arterial stenosis. Neurology. 2018;90(6):e447e454.

    • Search Google Scholar
    • Export Citation
  • 38

    Kang K, Gao F, Mo D, Yang M, Liu Y, Yang B, et al. Outcome of endovascular recanalization for intracranial in-stent restenosis. J Neurointerv Surg. 2020;12(11):10941098.

    • Search Google Scholar
    • Export Citation
  • 39

    Trossbach M, Hartmann M, Braun C, Sartor K, Hähnel S. Small vessel stents for intracranial angioplasty: in vitro evaluation of in-stent stenoses using CT angiography. Neuroradiology. 2004;46(6):459463.

    • Search Google Scholar
    • Export Citation
  • 40

    Psychogios MN, Schramm P, Amelung N, Pilgram-Pastor SM, Gröschel K, Wasser K, et al. Evaluation of noninvasive follow-up methods for the detection of intracranial in-stent restenosis: a phantom study. Invest Radiol. 2013;48(2):98103.

    • Search Google Scholar
    • Export Citation
  • 41

    Drachman DE, Edelman ER, Seifert P, Groothuis AR, Bornstein DA, Kamath KR, et al. Neointimal thickening after stent delivery of paclitaxel: change in composition and arrest of growth over six months. J Am Coll Cardiol. 2000;36(7):23252332.

    • Search Google Scholar
    • Export Citation
  • 42

    Zhang J, Zhang X, Zhang J, Song Y, Zheng M, Sun L, et al. Drug-coated balloon dilation compared with conventional stenting angioplasty for intracranial atherosclerotic disease. Neurosurgery. 2020;87(5):992998.

    • Search Google Scholar
    • Export Citation
  • 43

    Ridker PM, Cannon CP, Morrow D, Rifai N, Rose LM, McCabe CH, et al. C-reactive protein levels and outcomes after statin therapy. N Engl J Med. 2005;352(1):2028.

    • Search Google Scholar
    • Export Citation
  • 44

    Ridker PM, Everett BM, Thuren T, MacFadyen JG, Chang WH, Ballantyne C, et al. Antiinflammatory therapy with canakinumab for atherosclerotic disease. N Engl J Med. 2017;377(12):11191131.

    • Search Google Scholar
    • Export Citation

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