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Year : 2014  |  Volume : 27  |  Issue : 2  |  Page : 426-431

Reliability and sensitivity of transcranial Doppler in the prediction of recurrence in ischemic stroke

Department of Neuropsychiatry, Menoufiya University, Menoufiya, Egypt

Date of Submission02-Sep-2013
Date of Acceptance19-Oct-2013
Date of Web Publication26-Sep-2014

Correspondence Address:
Ahmed M Ateya
MBBCh, 7 Taha Kandil St., Matareya Square, Matareya Teaching Hospital, Department of Neuropsychiatry, Cairo - 3919
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/1110-2098.141721

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This study was designed to evaluate the role of serial transcranial Doppler (TCD) examinations in the prediction of early recurrence in acute cerebral ischemia (ACI).
In patients with ACI, either transient ischemic attack or acute ischemic stroke, the risk of early recurrence is significant. TCD enables the examination of hemodynamic patterns of intracranial circulation blood flow. After transient ischemic attack or acute ischemic stroke, developing cerebral flow hemodynamics is related to the stroke outcome.
Materials and methods
A prospective trial was performed on 60 patients with the first ever or second-time ACI affecting the anterior circulation territory. A diagnostic work up including full clinical examination, routine laboratory tests, brain computed tomography, and TCD examination were performed to evaluate the risk factors of recurrence. Patients were followed up by clinical and TCD examination for 90 days after ischemia (days 2, 7, 30, and 90) to detect clinical and hemodynamic evidences of correlated with early recurrence.
Patients were divided into two groups [group A with early recurrence (n = 12) and group B without early recurrence (n = 48)]. Diabetes mellitus, atrial fibrillation, and a history of cerebrovascular ischemia were found to be significantly associated with early recurrence of ischemia (P < 0.05). Initial TCD parameters showed that about 75% of the study patients had an abnormally increased mean arterial flow velocity (MFV) of the intracranial artery supplying the affected vascular territory. Group A patients tended to have a higher MFV (M = 77 ± 11.7) than group B patients (M = 66.47 ± 15.3) with significant effect (P < 0.05). Microembolic signals were detected in 10/12 patients (83%) with early recurrence, showing a significant relationship (P < 0.001).
Our results indicate that TCD parameters of intracranial hemodynamics, especially increasing MFV of the affected intracranial arteries and detection of microembolic signals, are of predictive value in risk stratification of early recurrence in patients with ACI.

Keywords: Ischemic stroke, recurrence, transcranial Doppler

How to cite this article:
Okda MA, El-Sheikh WM, El-Shereef AM, Ateya AM. Reliability and sensitivity of transcranial Doppler in the prediction of recurrence in ischemic stroke. Menoufia Med J 2014;27:426-31

How to cite this URL:
Okda MA, El-Sheikh WM, El-Shereef AM, Ateya AM. Reliability and sensitivity of transcranial Doppler in the prediction of recurrence in ischemic stroke. Menoufia Med J [serial online] 2014 [cited 2020 Jun 1];27:426-31. Available from: http://www.mmj.eg.net/text.asp?2014/27/2/426/141721

  Introduction Top

The traditional definition of stroke, devised by the WHO in the 1970s, is a 'neurological deficit of cerebrovascular cause that persists beyond 24 h or is interrupted by death within 24 h'. This definition was supposed to reflect the reversibility of tissue damage and was devised for the purpose, with the time frame of 24 h being chosen arbitrarily. The 24-h limit differentiates stroke from transient ischemic attack (TIA), which is a related syndrome of stroke symptoms that resolve completely within 24 h [1].

Stroke is the second cause of death, preceded only by heart diseases, with significant morbidity and mortality. In Egypt, the incidence of stroke was found to be 2.1 per 1000 population, whereas the prevalence was 5.4 per 1000 population [2].

According to Keerthi et al. [3], recurrent ischemic stroke is the same as for the primary event with an additional criterion: 'There had to be either a new neurological deficit or a deterioration of the previous deficit not considered to be due to edema, hemorrhagic transformation, or intercurrent illness'. The 90-day risk of a subsequent stroke after a TIA or an acute ischemic stroke (AIS) is approximately as high as 10-20%.

Transcranial Doppler (TCD), which became available in 1982, is a noninvasive ultrasonic technique that uses a hand-held low-frequency sector transducer that sends fixed or pulsed sound waves to measure the velocity of blood flowing in the basal intracranial arteries of the brain [4]. Hence, normal flow velocity can be easily distinguished from the accelerated velocities associated with vasospasm, arterial stenosis, and arteriovenous malformation. An advantage of TCD is that it can be performed at the bedside and repeated as needed or applied for continuous monitoring [5].

Markus et al. [6] and Alice and Hugh [7] found that TCD can help predict early stroke and recurrent TIA risk by detecting microembolic signals (MES), which are most frequently seen in patients with unstable atherosclerotic carotid plaques. These MES are frequently found early in the time course after acute stroke onset. Furthermore, MES represent an independent predictor of early ischemic recurrence when the cause appears related to large-artery atherosclerosis (e.g. carotid or middle-cerebral artery stenosis) [6].

The role of intracranial hemodynamic parameters in relation to the stroke outcome has been assessed in specific patient groups. Sacco et al. [8] demonstrated with TCD that in 8% of 438 patients with ischemic stroke, intracerebral atherosclerosis was the most probable cause of the stroke. Internal carotid and middle-cerebral artery TCD flow velocity were good predictors of stroke risk in children with sickle cell disease [9]. Also, the progression of symptomatic middle-cerebral artery occlusion monitored with TCD was associated with an increased risk of (recurrent) stroke [10].

In this study, the association between TCD hemodynamic parameters and the risk of early recurrence in ischemic stroke were explored and tested.

  Materials and methods Top

A group of 60 patients admitted with cerebrovascular ischemia (CVI), either TIA or AIS, during the period from September 2011 to August 2012, were recruited for the study from inpatient wards or the Neuroscience Intensive Care Unit of Matareya Teaching Hospital, Matareya, Cairo, Egypt. The study patients were diagnosed with CVI (index event) affecting the carotid (anterior) vascular system in an emergency setting. The index event is defined as an acute CVI event (either TIA or AIS) upon which the patient was included in the study. The index event was either the first ever the patient had or the second to a past minor CVI event (i.e. either past TIA or past AIS with mild but no severe functional deficits).

Patients with hemorrhagic stroke, CVI affecting posterior circulation, a history of major/multiple ischemic strokes, or with a history of decompensated systemic illness were excluded from the study.

All patients underwent a full clinical and diagnostic work up, initial and follow-up (after 48 h) brain computed tomographic imaging to confirm the diagnosis and laboratory tests for the evaluation of cerebrovascular risk factors such as hypertension, diabetes mellitus, atrial fibrillation (AF), hyperlipidemia, smoking, history of coronary artery disease, and history of CVI.

TCD examination was performed using a DWL EZ-Dop machine (2006; Compumedics, Singen, Germany) at the time of presentation to assess the initial state of intracranial arterial flow hemodynamics. Intracranial vessels were examined by the transtemporal approach using a 2-MHz probe according to a standardized TCD insonation protocol to identify suspected arterial obstruction or stenosis. Identification of the examined intracranial arterial segments was carried out according to certified published TCD identification criteria [11]. Intracranial hemodynamic parameters such as the end-diastolic velocity, the peak systolic velocity, mean cerebral blood flow velocities (MFV), the resistivity index, and the pulsatility index (PI) were recorded automatically.

According to Mead et al. [12] and Limin et al. [13], a diagnosis of normal-velocity, hyperemic (diffuse velocity increase above normal limits along the length of the artery that could be insonated), occluded, or focal stenosis (a localized area of increased velocity above normal limits associated with turbulence) at the time of examination was made.

To detect MES, the spectral recording of TCD was obtained with minimal gain at a fixed angle of insonation. The criteria for the identification of MES were adopted from the Consensus Committee of the Ninth International Cerebral Hemodynamic Symposium [14].

The patients studied were followed up for 90 days after the index event at fixed intervals (days 2, 7, 30, and 90). In follow-up visits, patients were clinically examined and investigated for appropriate control of stroke recurrence risk factors. Follow-up TCD examinations were carried out at the same time to record early hemodynamic parameter changes in the intracranial circulation.

Clinical evidences suggesting recurrence were investigated and documented by brain-imaging studies. Early recurrences identified during 90 days after the index event in the same affected territory or clearly in another part of the brain were registered.

Gathered data were processed using SPSS version 19 (SPSS Inc., Chicago, Illinois, USA). P value less than 0.05 was considered statistically significant. The c2 -test, Student's t-test, and the relative-risk correlation test were used when appropriate.

All participants signed an informed consent after receiving the required information regarding the study. Confidentiality of all patients' data was ensured.

  Results Top

Sixty patients with confirmed acute cerebral ischemia, either TIA or AIS, were clinically and radiologically identified and recruited for our study. After 24 h of admission, 15 patients (25%) were diagnosed as having TIA and 45 patients (75%) as having AIS.

Follow-up of the study patients was determined for the next 90 days after the index event to record early recurrence of stroke. At the end of the follow-up period, 20% of the patients (group A, n = 12) developed clinically and radiologically evident early recurrence of AIS and 80% of the patients (group B, n = 48) did not. A summary of the patients' characteristics is shown in [Table 1].
Table 1: Distribution of clinical risk factors among the study patients

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Initial and follow-up patterns of intracranial hemodynamics of the study patients were observed with particular concern to changes occurring in the symptomatic intracranial artery affected by the ischemic event. Other hemodynamic changes were also noted in other intracranial arteries in response to primary changes of the affected arteries. [Table 2] summarizes the findings of initial and follow-up patterns of TCD assessment of MFV of the symptomatic intracranial artery circulation in the study patients. The distribution of MFV patterns detected at initial TCD showed a statistically significant distribution among the study patients (P<0.05) with about 75% of them having abnormally increased MFV signals (hyperemic, 45% and stenotic, 30%) of symptomatic intracranial arteries. This means that patients with acute CVI events tended to have abnormally increased MFV of intracranial arteries.

From [Table 2], 12/60 patients (20%) had early recurrence of AIS within 90 postindex events. A follow-up TCD examination of these patients was associated with persistent abnormally increased MFV in eight (67%) patients (hyperemic, n = 5 and stenotic, n = 3) with affected intracranial arteries, whereas it was associated with worsening of initial hemodynamic parameters in 33% (n = 4) of them.
Table 2: Initial transcranial Doppler findings and follow-up patterns of hemodynamics in the study patients

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In [Table 3], analysis of serial recordings of MFV of symptomatic intracranial arteries of the study patients revealed a significant association (P < 0.05) with early recurrence. The mean (M) of MFV differed significantly among the two groups. Thus, group A with early recurrence of stroke tended to have a higher MFV (M = 77 ± 11.7) than group B without early recurrence of stroke (M = 66.47 ± 15.3).
Table 3: Mean arterial flow velocities of the symptomatic intracranial arteries

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In this study, real-time detection of MES was possible in 22 of the total study patients during routine TCD follow-up along a 90-day postindex event. Ten of these patients (45.5%) developed evident early recurrence of AIS [Table 4].
Table 4: Distribution of microembolic signals among the study patients

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In [Table 4], estimated relative risks of stroke recurrence in relation to the presence of MES was analyzed. Our results showed that there was a highly significant relationship between MES detection and early recurrence (P < 0.001). Our estimated relative risk was 8.636 (odds ratio = 15). Thus, we concluded that individuals who are MES positive are eight times as likely to have recurrent stroke as individuals who are MES negative.

  Discussion Top

Risks of stroke recurrence

During follow-up of the study patients, about 20% (n = 12) of all patients recorded early recurrence of stroke during 90 days after the index event. This rate of recurrence is in keeping with those of Philippe et al. [15]and Angel et al. [16], whereas they suggested that the 90-day risk of a subsequent stroke after an acute TIA or AIS is approximately as high as 10-20%.

Association between risk factors and stroke recurrence

Several authors have investigated the effect of potentially modifiable risk factors on stroke recurrence to help target secondary preventative interventions. Their results have often been contradictory, which may be accounted for by small sample sizes and differences in the definitions of risk factors [17]. The best established risk factors associated with stroke recurrence in previous studies have been diabetes mellitus [18],[19], AF [17,20], and a history of CVI [21]. This is in keeping with the present study in which these factors reached significance.

In this study, hypertension, hyperlipidemia, smoking, and coronary artery disease were distributed equally in the study population without any significant distribution or relation to the occurrence of recurrence of ischemic stroke. Previous findings regarding these risk factors have been more heterogeneous; this may be related to different criteria for identification and methods of treatment [17].

Follow-up patterns of intracranial hemodynamics

Initial TCD assessment of patients in this study revealed an early evolution of intracranial hemodynamics after CVI in the majority of the patients. The distribution of MFV patterns at initial TCD assessment among the study patients showed a significant relationship with a tendency of intracranial arteries to acquire abnormal MFV patterns in an acute CVI event (hyperemic, 45% and stenotic, 30%). This confirms the concept that autoregulation seems increasingly impaired in the first few days after TIA or ischemic stroke (mainly affected side) with a higher risk for development of early recurrence [22].

Among patients with initial normal TCD results, six patients were diagnosed with lacunar ischemic infarction and the other nine patients were diagnosed as having TIA. In a study conducted by Alexandrov et al. [23], patients with TIA showed an initial normal TCD assessment in about 65% of the patients. In contrast, Mead et al. [12] reported that the evolution of intracranial arterial hemodynamics in response to CVI is related to the subtype of the cerebral ischemic event. Vincent et al. [24] found that very few individuals with lacunar infarctions had any detectable intracranial artery abnormalities.

Follow-up TCD examinations of the previous group (i.e. patients with initial normal MFV) showed worsening of the hemodynamic pattern in two patients, where MFV in the ipsilateral middle cerebral artery (MCA) increased asymmetrically between the cerebral hemisphere. These changes were related to the occurrence of early recurrence in these two patients. In a study conducted by Akopov and Whitman [25], they found that even when initial TCD studies do not demonstrate the evolution of intracerebral hemodynamics, follow-up TCD may predict either improvement or deterioration of these patients. In the same study, clinical deterioration and early recurrence of ischemia was found to be related to worsening of cerebral autoregulatory mechanisms and deficient collateral circulation, which cause early recurrence of ischemia.

Among 27/60 (45%) patients in this study, the initial MFV assessment showed an abnormally increased hyperemic flow pattern in symptomatic intracranial arteries. In 22 patients, improvement in the MFV was observed along the follow-up serial TCD examinations with normalization of flow patterns at the end. Similar cases were discussed by Akopov and Whitman [25] in which developing an initial intracranial hyperemia may represent a reactive postischemic transitory reaction. Recent studies showed that progressive deterioration of cerebral autoregulation in the first days after CVI is possible with the recovery of cerebral autoregulation and intracranial hemodynamics over the 3-month postindex event [22].

The follow-up TCD of the remaining five patients with initially hyperemic signals showed a persistent hyperemic signal. Follow-up of these patients' hemodynamics showed development of an increased PI in the ipsilateral symptomatic intracranial artery, which later corresponded to distal occlusion and clinical development of early recurrent ischemia. Persistent hyperemic signals may be explained by the more subtle increase in the flow velocity that reflects a more subtle, and likely a more generalized, arterial narrowing caused by atherosclerosis [25].

Among patients with an initial stenotic MFV pattern (n = 18/60), 16 patients showed a persistent stenotic signal along the serial follow-up TCD. It was associated with ipsilateral increased PI in three patients during the follow-up, denoting distal embolization with clinical evidences of early recurrence of ischemia. In the remaining two patients with an initial stenotic signal, follow-up TCD showed worsening of intracranial hemodynamics and progression to dampened flow in ipsilateral MCA branches with clinical evidence of early recurrence of ischemia. Wong et al. [26] showed that intracranial arterial stenotic lesions are dynamic and can evolve over time, with increasing or decreasing flow velocities and appearance of new collateral patterns, suggesting further hemodynamic compromise distal to the stenotic lesion, predicting new ipsilateral stroke or TIA.

Association between transcranial Doppler parameters and risk of stroke recurrence

Data comparing the means (M) of MFV of intracranial arteries between patients who developed early stroke recurrence and those who did not showed a significant difference between the two groups with a tendency for higher MFV in patients with early recurrence of stroke (P < 0.05). These are in keeping with results stated by Mead et al. [12], wherein the risk of early recurrence is increased with increasing MFV of ipsilateral symptomatic intracranial arteries. Intracranial atherosclerosis is responsible for up to 10% of TIA and strokes [27]. Also, intracranial large-artery atherothrombotic stenosis may be a source of unstable atherosclerotic plaque causing artery-to-artery embolism responsible for early recurrence of ischemia [10].

MES has been detected in between 9.3 and 71% of patients in the acute phase after TIA and ischemic stroke [28]. From the analyzed results, risk estimates of developing early recurrence of ischemic stroke with detection of MES came to be linked together with a highly significant independent relationship. Accordingly, patients with a positive MES are more prone to develop early stroke recurrence than those with a negative MES. These findings are in keeping with data on stroke literature, wherein Markus et al. [6] confirmed a highly significant association between the baseline MES frequency and the 90-day stroke/TIA risk.

  Conclusion Top

This study provides strong evidence that diabetes, AF, and a history of cerebral ischemia are associated with an increased risk of early recurrence. Also, TCD parameters of intracranial arterial hemodynamics, especially after TIA or AIS, with increasing MFV of the affected intracranial arteries and detection of MES are of predictive value in the risk stratification of early ipsilateral recurrence of ischemic stroke.

  Acknowledgements Top

Special thanks are extended to Dr. Magdy Khalaf (Head of Neuropsychiatry Department, Matareya Teaching Hospital) without his help and advice this research would not have been possible.

Conflicts of interest

There are no conflicts of interest.

  References Top

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  [Table 1], [Table 2], [Table 3], [Table 4]


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