Microembolic Signals on Transcranial Doppler Ultrasonography: A Narrative Review of a Decade of Evidence

Article information

J Neurosonol Neuroimag. 2024;16(2):63-70
Publication date (electronic) : 2024 December 31
doi : https://doi.org/10.31728/jnn.2024.00165
Department of Neurology, Chung-Ang University Gwangmyeong Hospital, Gwangmyeong, Korea
Correspondence: JoonNyung Heo, MD, PhD Department of Neurology, Chung- Ang University Gwangmyeong Hospital, 501 Iljik-dong, Gwangmyeong 14353, Korea Tel: +82-2-2222-6627 Fax: +82-2-2610-6630 E-mail: jnheo@jnheo.com
Received 2024 November 21; Revised 2024 December 9; Accepted 2024 December 10.

Abstract

Microembolic signals (MESs), detected via transcranial Doppler ultrasonography, are essential biomarkers for assessing cerebrovascular risk, embolic events, and treatment outcomes. In this review, studies published between 2014 and 2024 were evaluated, specifically focusing on the clinical implications, associated conditions, and opportunities for advancements in MES monitoring technologies. A systematic PubMed search identified 327 articles, of which 60 were finally included in this review. MESs are associated with various conditions, including carotid/cerebral artery stenosis and atrial fibrillation. They predict adverse outcomes, including increased stroke risk, cognitive decline, and complications from procedures such as endovascular thrombectomy and unruptured aneurysm coiling. Furthermore, MESs serve as a surrogate marker for embolism, allowing for the evaluation of different procedural techniques to determine which approach minimizes embolic events. Advances in MES monitoring, including algorithms that distinguish gaseous and solid emboli and applications in pediatric cardiac surgery, have expanded its clinical utility. Moreover, emerging wearable and wireless technologies may expand the possibilities for MES monitoring.

INTRODUCTION

Microembolic signals (MESs), detected via transcranial Doppler ultrasonography, play a pivotal role in diagnosis and monitoring of cerebrovascular diseases. Unlike imaging modalities, such as magnetic resonance imaging or computed tomography, MESs offer real-time insights into embolic events, providing unique clinical and prognostic information. This capability has made MESs an invaluable tool for assessing the risk of stroke, understanding embolic complications, and evaluating the effectiveness of therapeutic interventions in both routine and specialized clinical settings.

The clinical and research landscape surrounding MESs has evolved significantly over the past decade, driven by advancements in diagnostic technologies and an increasing understanding of their role in cerebrovascular and systemic conditions. MESs have emerged as a critical biomarker for evaluating embolic risk, thereby guiding therapeutic decisions and predicting outcomes across a wide range of patient populations and clinical scenarios. This review aimed to summarize the findings from the past decade, providing a comprehensive overview of the current state of knowledge regarding MESs. By consolidating these insights, this review seeks to propose future directions to enhance the clinical utility of MESs as a diagnostic and prognostic tool in modern medicine.

BASIC CHARACTERISTICS OF MES

The Basic Identification Criteria of Doppler Microembolic Signals established by the Consensus Committee of the Ninth International Cerebral Hemodynamic Symposium in 1995 remain largely unchanged and continue to serve as the foundation for identifying MESs.1 These criteria define MESs as unidirectional short-duration signals (<300 ms), with significant increases in intensity (>3 dB) above the background blood flow, occurring randomly throughout the cardiac cycle and producing a characteristic audible sound (often described as a “whistle,” “chirp,” or “click”). However, for heightened specificity, some studies have incorporated a higher threshold, such as a 9.0 dB threshold.2,3

LITERATURE SEARCH

A systematic literature search was conducted using PubMed to identify studies related to MESs. The search utilized the terms “(Microembolic [Title] OR (high-intensity transient [Title]))” and included results published between January 2014 and October 2024. To ensure relevance and quality, the following exclusion criteria were applied after reviewing titles and abstracts: non-clinical research articles (e.g., reviews, meta-analyses, clinical trial protocols, editorials, and case reports), studies conducted on non-human subjects, articles unrelated to transcranial Doppler sonography, and those not focused on MES.

A total of 327 articles met the criteria for the search terms and of these articles, 95 were published between January 2014 and October 2024 (Fig. 1). From these 95 articles, 60 were finally included after the exclusion of 35 articles (17 non-clinical articles, 8 studies involving non-human subjects, 2 articles unrelated to transcranial Doppler sonography, and 5 articles not focused on MESs). A schematic representation of the key topics of the included articles is provided in Fig. 2.

Fig. 1.

Flow diagram of articles included for review.

Fig. 2.

Schematic representation of key topics of the included articles. MES, microembolic signal; MCA, middle cerebral artery.

FACTORS ASSOCIATED WITH THE PRESENCE OF MES

MESs are more frequently observed in cases with significant stenosis in the extracranial carotid artery and middle cerebral artery.4,5 Stenosis involving these arteries creates areas of turbulent and disrupted blood flow, which increases shear stress and can damage the endothelial lining of blood vessel walls.6,7 This endothelial injury promotes platelet activation and aggregation, as well as the formation of microthrombi. Furthermore, the narrowed arterial lumen increases the likelihood of embolization as fragments of atherosclerotic plaque or thrombi detach and travel distally. These microemboli, formed through a combination of plaque rupture, thrombus formation, and local hemodynamic changes, are detected as MESs.8 Vulnerable extracranial carotid plaques, represented by lipid-rich plaques or luminal thrombi upon histopathological examination after a carotid endarterectomy, are associated with MESs.9 MES frequency during carotid endarterectomy is associated with vulnerable characteristics in plaque magnetic resonance imaging.10 However, plaque characteristics on magnetic resonance imaging are not associated with MESs in patients with mild-to-moderate symptomatic plaques.11 MESs are more commonly detected in cases with a short delay between stroke onset and monitoring, as well as in cases of symptomatic stenosis compared to asymptomatic lesions, affecting both intracranial and extracranial arteries.5,7,12 The use of dual antiplatelet therapy or statins prior to a stroke, particularly in patients with large artery atherosclerosis, is associated with a decreased MES frequency, suggesting a role in plaque stabilization.13-15

Underlying conditions, such as atrial fibrillation, are also known to be associated with MESs.16 Patients who experienced an embolic stroke with undetermined etiology show a higher frequency of MESs than those with other etiologies.17 MESs are also detected in patients with essential thrombosis or insulin resistance.18,19 Additionally, they are more frequent in patients who experience migraines with higher cortical dysfunction during aura than in healthy controls and in those with only visual or somatosensory symptoms.20 However, these associations were based on limited evidence from single-center studies, and a direct causal relationship has not been established. Patients who had higher cortical dysfunction, such as language and memory impairment, during aura had more frequent MESs than the other control groups (29.4% vs. 3.2% and 5.9%).

CLINICAL IMPLICATIONS OF MES

MESs have been increasingly recognized as a valuable biomarker for predicting stroke risk, assessing disease progression, and guiding therapeutic interventions. MESs have been linked to an increased risk of stroke in the future and poorer outcomes in patients who have experienced an ischemic stroke or transient ischemic attack.2 In a meta-analysis, there was a two-fold increase in the chance of a new cerebral infarction when MESs were detected. 21 Specifically, not only stroke recurrence (hazard ratio 4.90) but functional disability (discharge-modified Rankin Scale 3–6, odds ratio 3.3) and longer hospital stays (approximately 3 days more) were associated with MESs. A similar association was also observed in patients who experienced strokes due to large artery occlusion, who underwent endovascular thrombectomies.22 Notably, MESs were detected in 65% of patients who underwent EVT, more frequently in patients with ipsilateral carotid stenosis, carotid occlusion, or inadequate or no collaterals. The presence MESs after thrombectomy are associated with a significantly higher incidence of composite vascular events (odds ratio 4.85) and worse functional outcomes at a threshold of 5 MESs per hour (3 month modified Rankin Scale >2, 76.9% vs. 34.7%). The risk of cognitive decline was also associated with the presence of MESs in patients with neurological disorders.23

MESs may also be used to assess the embolic risk of underlying diseases. MESs are found more frequently in patients with moyamoya disease who experienced recent ischemic events and are predictive of future ischemic events, suggesting a potential link between MESs and stroke risk in moyamoya disease.24-26 A change to an antiplatelet therapy regimen was evaluated in patients with moyamoya disease who had MESs (21 patients).26 Follow-up monitoring showed loss of MESs for all patients after the antiplatelet regimen change, underscoring MESs as a biomarker for guiding antiplatelet therapy. Similarly, patients with atrial fibrillation who exhibit MESs are associated with a higher risk of embolism.16 Patients with active cancer and acute stroke are at risk for increased mortality and infarction involving multiple arterial territories if MESs are detected during monitoring.27 MESs are also related with ischemic complications after unruptured intracranial aneurysm coiling.28 They can be detected in 65.7% of patients immediately after coiling and in 36.8% of patients 24 hours post-coiling. The presence of MESs at both time points show a strong correlation with the number of ischemic lesions identified on magnetic resonance imaging. This was a single-center study involving 45 patients, and further validation is required.

USE OF MES AS AN EMBOLISM MARKER

MESs can serve as a surrogate marker for embolism, particularly in scenarios where embolic complications, such as stroke, occur infrequently. For example, MES monitoring during high embolic risk procedures allows for the evaluation of different procedural techniques to determine which approach minimizes embolic events. This methodology enables statistically significant findings to be achieved with smaller sample sizes. Numerous studies have been published regarding assessment of embolic risk during catheter ablation for atrial fibrillation.29-33 Embolic risk differences between procedural techniques were assessed using MESs during transcatheter aortic valve implantation.34-36 MESs have been utilized as a marker for plaque stability in evaluating imaging modalities such as FDG-PET CT, contrast-enhanced ultrasound, and Superb Microvascular Imaging ultrasound.37-39 They have also been employed to assess embolism risk using laboratory values as predictors, such as C-reactive protein, osteoprotegerin, and CXCL16 cytokine levels.40-42 The influence of genetic polymorphisms in PTPN22, NLRP3, and OPG genes on embolism risk has been studied using MESs.43-45 Additionally, MES have been used to understand the impact of platelet reactivity on embolic risk in carotid stenosis.46-48

LIMITATIONS OF MES

Despite the frequent detection of MESs during specific medical and surgical interventions, several studies have reported no significant association with clinical outcomes. For instance, MESs observed during carotid endarterectomy do not correlate with the development of new brain lesions post-procedure, possibly due to the small number of events (4 out of 160 patients).49 Similarly, while MESs are commonly detected during pulmonary vein isolation and are known to be associated with brain lesions or neurologic outcomes,29,50 they were not linked to silent brain lesions, cognitive changes, or stroke in one multicenter study.51 Additionally, although cognitive dysfunction is commonly noted following left heart catheterization, it is not associated with the number of microemboli detected during the procedure.52 These results may imply that, in cardiac procedures, neurologic outcomes may be influenced not only by the MES count, but also by procedural or individual factors.

EXTENDED APPLICATIONS IN SPECIALIZED POPULATIONS

Recent advancements have expanded the use of MES monitoring into specialized clinical contexts. In infants undergoing cardiac catheterization and surgery, MES monitoring has been successfully performed, providing insights into cerebral embolic risks during these procedures.53,54 However, MESs detected during infant cardiac surgery is not directly linked to specific surgical maneuvers.55 Furthermore, a novel algorithm capable of differentiating gaseous from solid embolic signals has been developed, potentially enhancing MES monitoring during cardiac surgeries.56 MES detection at the vertebrobasilar junction in patients with vertebral artery dissection was previously performed, implying MES monitoring at the vertebrobasilar junction as a feasible option.57

FUTURE DIRECTIONS

Recent studies surrounding MESs indicate the clinical potential of transcranial monitoring for MESs. MES detection provides critical insights into the risk of stroke, embolic complications, and plaque stability, making it an indispensable tool in various clinical scenarios. However, its utility is currently limited by practical constraints, including the expertise required for interpretation and the short duration of monitoring.58,59 As a result, MES monitoring is not performed as frequently as its clinical potential might warrant. Advanced wearable and wireless technologies may present an exciting opportunity to overcome these limitations.60 Portable devices for long-term MES monitoring may enhance early detection of embolic events and broaden their clinical utility. By improving accessibility and enabling outpatient use, these advancements may support more comprehensive monitoring and personalized management of embolic risks, although further research is needed.

Notes

Ethics Statement

Institutional Review Board approval and patient consent were not necessary because this is a review article.

Availability of Data and Material

The data supporting the findings of this study are available from the corresponding author on request.

Sources of Funding

None.

Conflicts of Interest

No potential conflicts of interest relevant to this article was reported.

Acknowledgements

None.

References

1. Basic identification criteria of Doppler microembolic signals. Consensus Committee of the Ninth International Cerebral Hemodynamic Symposium. Stroke 1995;26:1123.
2. Das AS, Regenhardt RW, LaRose S, Monk AD, Castro PM, Sheriff FG, et al. Microembolic signals detected by transcranial Doppler predict future stroke and poor outcomes. J Neuroimaging 2020;30:882–889.
3. Hashemilar M, Farhoudi M, Hosseini S, Moshayedi H, Savadi Oskoui D, et al. Frequency of microembolic signals in patients with acute ischemic stroke in middle cerebral artery territory treated with aspirin or clopidogrel. Iran J Neurol 2011;10:16–18.
4. Medvedkova EY, Berdalin AB, Orlova EV, Lelyuk VG. Microembolic signals in arteries of the base of the brain after ischemic stroke. Bull Exp Biol Med 2022;173:193–198.
5. Chen X, Liu K, Wu X, Wang S, Li T, Xing Y. Microembolic signals predict recurrence of ischemic events in symptomatic patients with middle cerebral artery stenosis. Ultrasound Med Biol 2018;44:747–755.
6. Wong KS, Gao S, Chan YL, Hansberg T, Lam WW, Droste DW, et al. Mechanisms of acute cerebral infarctions in patients with middle cerebral artery stenosis: a diffusion-weighted imaging and microemboli monitoring study. Ann Neurol 2002;52:74–81.
7. Wu X, Zhang H, Liu H, Xing Y, Liu K. Microembolic signals detected with transcranial doppler sonography differ between symptomatic and asymptomatic middle cerebral artery stenoses in Northeast China. PLoS One 2014;9e88986.
8. Ritter MA, Dittrich R, Thoenissen N, Ringelstein EB, Nabavi DG. Prevalence and prognostic impact of microembolic signals in arterial sources of embolism. A systematic review of the literature. J Neurol 2008;255:953–961.
9. Van Lammeren GW, Van De Mortel RH, Visscher M, Pasterkamp G, De Borst GJ, et al. Spontaneous preoperative microembolic signals detected with transcranial Doppler are associated with vulnerable carotid plaque characteristics. J Cardiovasc Surg (Torino) 2014;55:375–380.
10. Sato Y, Ogasawara K, Narumi S, Sasaki M, Saito A, Tsushima E, et al. Optimal MR plaque imaging for cervical carotid artery stenosis in predicting the development of microembolic signals during exposure of carotid arteries in endarterectomy: Comparison of 4 T1-weighted imaging techniques. AJNR Am J Neuroradiol 2016;37:1146–1154.
11. Truijman MT, de Rotte AA, Aaslid R, van Dijk AC, Steinbuch J, Liem MI, et al. Intraplaque hemorrhage, fibrous cap status, and microembolic signals in symptomatic patients with mild to moderate carotid artery stenosis: the Plaque at RISK study. Stroke 2014;45:3423–3426.
12. Bazan R, Luvizutto GJ, Braga GP, Bazan SGZ, Hueb JC, de Freitas CCM, et al. Relationship of spontaneous microembolic signals to risk stratification, recurrence, severity, and mortality of ischemic stroke: a prospective study. Ultrasound J 2020;12:6.
13. Safouris A, Katsanos AH, Kerasnoudis A, Krogias C, Kinsella JA, Sztajzel R, et al. Statin pretreatment and microembolic signals in large artery atherosclerosis. Stroke 2018;49:1992–1995.
14. Deng QQ, Tang J, Chen C, Markus H, Huang YN, Zhao H, et al. The curative effect comparison of two kinds of therapeutic regimens on decreasing the relative intensity of microembolic signal in CLAIR trial. J Neurol Sci 2016;367:18–21.
15. Lau AY, Zhao Y, Chen C, Leung TW, Fu J, Huang Y, et al. Dual antiplatelets reduce microembolic signals in patients with transient ischemic attack and minor stroke: subgroup analysis of CLAIR study. Int J Stroke 2014;9 Suppl A100:127–132.
16. Xu Y, Dong ZZ, Jiang LJ, Zhang CX, Dong GY. Analysis of Variables Associated with positive micro-embolic signals detected by transcranial doppler in patients with atrial fibrillation and their predictive value for embolic risk. Risk Manag Healthc Policy 2023;16:2439–2444.
17. Higuchi E, Toi S, Shirai Y, Hoshino T, Ishizuka K, Shimizu S, et al. Prevalence of microembolic signals in embolic stroke of undetermined source and other subtypes of ischemic stroke. Stroke 2020;51:655–658.
18. Cinar A, Cetin G, Altintas Kadirhan O, Turgut S, Ekinci I, Asil T. Determination of cerebral blood flow velocity and microembolic signals in essential thrombocytosis by transcranial doppler ultrasonography. Neurol Res 2021;43:157–163.
19. Zhou X, Zhang D, Zhou Y, Wang F, Zhu X. Microembolic signals is associated with insulin resistance among acute ischemic stroke patients. J Stroke Cerebrovasc Dis 2019;28:1070–1077.
20. Petrusic I, Podgorac A, Zidverc-Trajkovic J, Radojicic A, Jovanovic Z, Sternic N. Do interictal microembolic signals play a role in higher cortical dysfunction during migraine aura? Cephalalgia 2016;36:561–567.
21. King A, Markus HS. Doppler embolic signals in cerebrovascular disease and prediction of stroke risk: a systematic review and meta-analysis. Stroke 2009;40:3711–3717.
22. Farina F, Palmieri A, Favaretto S, Viaro F, Cester G, Causin F, et al. Prognostic role of microembolic signals after endovascular treatment in anterior circulation ischemic stroke patients. World Neurosurg 2018;110:e882–e889.
23. Yan J, Li Z, Wills M, Rajah G, Wang X, Bai Y, et al. Intracranial microembolic signals might be a potential risk factor for cognitive impairment. Neurol Res 2021;43:867–873.
24. Jeon C, Yeon JY, Jo KI, Hong SC, Kim JS. Clinical role of microembolic signals in adult Moyamoya disease with ischemic stroke. Stroke 2019;50:1130–1135.
25. Chen J, Duan L, Xu WH, Han YQ, Cui LY, Gao S. Microembolic signals predict cerebral ischaemic events in patients with moyamoya disease. Eur J Neurol 2014;21:785–790.
26. Pompsch M, Veltkamp R, Diehl RR, Kraemer M. Microembolic signals and antiplatelet therapy in Moyamoya angiopathy. J Neurol 2022;269:6605–6612.
27. Toi S, Higuchi E, Hosoya M, Arai S, Ishizuka K, Mizuno T, et al. Association of transcranial Doppler microembolic signal with short-term mortality in acute ischemic stroke and active cancer. J Am Heart Assoc 2024;13e033634.
28. Cho JH, Kang DH, Kim YW, Park J, Kim YS. Microembolic signal monitoring and the prediction of thromboembolic events following coil embolization of unruptured intracranial aneurysms: diffusion-weighted imaging correlation. Neuroradiology 2015;57:189–196.
29. Mizutani Y, Yanagisawa S, Ichikawa M, Nishio K, Sakai H, Nonokawa D, et al. Evaluation of microembolic signals on carotid ultrasound during pulmonary vein isolation with high-power short-duration and cryoballoon ablations: When and where do bubble and solid emboli arise? J Cardiovasc Electrophysiol 2024;35:1589–1600.
30. Christoph M, Poitz D, Pfluecke C, Forkmann M, Huo Y, Gaspar T, et al. Simple periprocedural precautions to reduce Doppler microembolic signals during AF ablation. J Interv Card Electrophysiol 2022;64:359–365.
31. von Bary C, Deneke T, Arentz T, Schade A, Lehrmann H, Fredersdorf S, et al. Online measurement of microembolic signal burden by transcranial Doppler during catheter ablation for atrial fibrillation-results of a multicenter trial. Front Neurol 2017;8:131.
32. Larbig R, Dittrich R, Kochhaeuser S, Leitz P, Guener F, Korsukewitz C, et al. Influence of clinical parameters and anticoagulation on intraprocedural cerebral microembolic signals during pulmonary vein isolation. PLoS One 2016;11e0157886.
33. Zellerhoff S, Ritter MA, Kochhäuser S, Dittrich R, Köbe J, Milberg P, et al. Modified phased radiofrequency ablation of atrial fibrillation reduces the number of cerebral microembolic signals. Europace 2014;16:341–346.
34. Vavuranakis MA, Kalantzis C, Voudris V, Kosmas E, Kalogeras K, Katsianos E, et al. Comparison of ticagrelor versus clopidogrel on cerebrovascular microembolic events and platelet inhibition during transcatheter aortic valve implantation. Am J Cardiol 2021;154:78–85.
35. Aratake S, Kayama S, Watanabe Y, Honjo T, Harada M, Onimaru T, et al. High-intensity transient signals during transcatheter aortic valve implantation assessed by ultrasonic carotid artery blood-flow monitoring: A single center prospective observational study. J Cardiol 2020;76:244–250.
36. Erdoes G, Huber C, Basciani R, Stortecky S, Windecker S, Wenaweser P, et al. The self-expanding Symetis Acurate does not increase cerebral microembolic load when compared to the balloon-expandable Edwards Sapien prosthesis: a transcranial Doppler study in patients undergoing transapical aortic valve implantation. PLoS One 2014;9e108191.
37. Müller HF, Viaccoz A, Fisch L, Bonvin C, Lovblad KO, Ratib O, et al. 18FDG-PET-CT: an imaging biomarker of high-risk carotid plaques. Correlation to symptoms and microembolic signals. Stroke 2014;45:3561–3566.
38. Chiba T, Fujiwara S, Oura K, Oikawa K, Chida K, Kobayashi M, et al. Superb microvascular imaging ultrasound for cervical carotid artery stenosis for prediction of the development of microembolic signals on transcranial Doppler during carotid exposure in endarterectomy. Cerebrovasc Dis Extra 2021;11:61–68.
39. Oikawa K, Kato T, Oura K, Narumi S, Sasaki M, Fujiwara S, et al. Preoperative cervical carotid artery contrast-enhanced ultrasound findings are associated with development of microembolic signals on transcranial Doppler during carotid exposure in endarterectomy. Atherosclerosis 2017;260:87–93.
40. Foroughinia F, Tabibi AA, Javanmardi H, Safari A, Borhani-Haghighi A. Association between high sensitivity C-reactive protein (hs-CRP) levels and the risk of major adverse cardiovascular events (MACE) and/or microembolic signals after carotid angioplasty and stenting. Caspian J Intern Med 2019;10:388–395.
41. Cao Y, Cui C, Zhao H, Pan X, Li W, Wang K, et al. Plasma osteoprotegerin correlates with stroke severity and the occurrence of microembolic signals in patients with acute ischemic stroke. Dis Markers 2019;2019:3090364.
42. Ma A, Yang S, Wang Y, Wang X, Pan X. Increase of serum CXCL16 level correlates well to microembolic signals in acute stroke patients with carotid artery stenosis. Clin Chim Acta 2016;460:67–71.
43. Zhou L, Wang K, Wang J, Zhou Z, Cheng Y, Pan X, et al. PTPN22 Gene polymorphisms are associated with susceptibility to large artery atherosclerotic stroke and microembolic signals. Dis Markers 2019;2019:2193835.
44. Cheng L, Yin R, Yang S, Pan X, Ma A. Rs4612666 Polymorphism of the NLRP3 gene is associated with the occurrence of large artery atherosclerotic ischemic strokes and microembolic signals. Biomed Res Int 2018;2018:6345805.
45. Zhao H, Cao Y, Chen H, Xu W, Sun X, Pan X. The association between OPG rs3102735 gene polymorphism, microembolic signal and stroke severity in acute ischemic stroke patients. Gene 2017;613:25–29.
46. Kinsella JA, Oliver Tobin W, Tierney S, Feeley TM, Egan B, Coughlan T, et al. Assessment of ‘on-treatment platelet reactivity’ and relationship with cerebral micro-embolic signals in asymptomatic and symptomatic carotid stenosis. J Neurol Sci 2017;376:133–139.
47. Murphy SJX, Lim ST, Kinsella JA, Tierney S, Egan B, Feeley TM, et al. Relationship between ‘on-treatment platelet reactivity’, shear stress, and micro-embolic signals in asymptomatic and symptomatic carotid stenosis. J Neurol 2020;267:168–184.
48. Murphy SJ, Lim ST, Kinsella JA, Tierney S, Egan B, Feeley TM, et al. Simultaneous assessment of plaque morphology, cerebral micro-embolic signal status and platelet biomarkers in patients with recently symptomatic and asymptomatic carotid stenosis. J Cereb Blood Flow Metab 2020;40:2201–2214.
49. Kim C, Lee J, Lee SJ, Yun WS. Intraoperative microembolic signals during carotid endarterectomy. Ann Vasc Surg 2022;81:196–201.
50. Kochhäuser S, Lohmann HH, Ritter MA, Leitz P, Güner F, Zellerhoff S, et al. Neuropsychological impact of cerebral microemboli in ablation of atrial fibrillation. Clin Res Cardiol 2015;104:234–240.
51. von Bary C, Deneke T, Arentz T, Schade A, Lehrmann H, Schwab-Malek S, et al. Clinical impact of the microembolic signal burden during catheter ablation for atrial fibrillation: Just a lot of noise? J Ultrasound Med 2018;37:1091–1101.
52. Scott DA, Evered LA, Gerraty RP, MacIsaac A, Lai-Kwon J, Silbert BS. Cognitive dysfunction follows left heart catheterisation but is not related to microembolic count. Int J Cardiol 2014;175:67–71.
53. Leth-Olsen M, Døhlen G, Torp H, Nyrnes SA. Detection of cerebral high-intensity transient signals by NeoDoppler during cardiac catheterization and cardiac surgery in infants. Ultrasound Med Biol 2022;48:1256–1267.
54. LaRovere KL, Kapur K, McElhinney DB, Razumovsky A, Kussman BD. Cerebral high-intensity transient signals during pediatric cardiac catheterization: A pilot study using transcranial doppler ultrasonography. J Neuroimaging 2017;27:381–387.
55. Twedt MH, Hage BD, Hammel JM, Ibrahimye AN, Shukry M, Qadeer A, et al. Most high-intensity transient signals are not associated with specific surgical maneuvers. World J Pediatr Congenit Heart Surg 2020;11:401–408.
56. Keunen RWM, Daal SM, Romers GJ, Hoohenkerk GJF, van Kampen PM, Suyker WJL. Diagnostic accuracy of an algorithm for discriminating presumed solid and gaseous microembolic signals during transcranial doppler examinations. Ultrasound Med Biol 2023;49:2483–2488.
57. Yamaoka Y, Ichikawa Y, Kimura T, Sameshima T, Ochiai C, Morita A. A novel method for transcranial Doppler microembolic signal monitoring at the vertebrobasilar junction in vertebral artery dissection patients. J Neuroimaging 2014;24:191–194.
58. Sharma VK, Wong KS, Alexandrov AV. Transcranial Doppler. Front Neurol Neurosci 2016;40:124–140.
59. Mackinnon AD, Aaslid R, Markus HS. Long-term ambulatory monitoring for cerebral emboli using transcranial Doppler ultrasound. Stroke 2004;35:73–78.
60. Pietrangelo SJ, Lee HS, Sodini CG. A Wearable transcranial Doppler ultrasound phased array system. Acta Neurochir Suppl 2018;126:111–114.

Article information Continued

Fig. 1.

Flow diagram of articles included for review.

Fig. 2.

Schematic representation of key topics of the included articles. MES, microembolic signal; MCA, middle cerebral artery.