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 Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 7  |  Issue : 3  |  Page : 274-281

Transcranial Doppler to detect early abnormalities in cerebral hemodynamics following traumatic brain injury in adult patients


Department of Anesthesia and Intensive Care, Faculty of Medicine, Zagazig University, Zagazig, Egypt

Date of Submission03-Feb-2018
Date of Acceptance18-Dec-2018
Date of Web Publication29-Sep-2020

Correspondence Address:
Amani A Aly
Department of Anesthesia and Intensive Care, Faculty of Medicine, Zagazig University, 54, 2nd Region, 2nd District, 5th Settlement, New Cairo, Cairo
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/roaic.roaic_7_18

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  Abstract 

Background Transcranial Doppler (TCD) can be a valuable tool in detecting early changes in cerebral blood flow (CBF) velocities following traumatic brain injury (TBI). We designed this prospective observational study to screen for early abnormalities in CBF following TBI using TCD and to evaluate its ability to predict the patients’ outcome.
Patients and methods The study was carried out on 66 adult patients admitted to the ICU with TBI. TCD was performed on admission by insonating the middle cerebral arteries and extracranial internal carotid arteries, and flow velocities were recorded, and pulsatility index (PI) and Lindegaard ratio were calculated. End-diastolic velocity (EDV) less than 25 cm/s and PI more than 1.3 were considered abnormal. The patient outcome was evaluated at discharge from the hospital using the Glasgow Outcome Scale.
Results Admission TCD revealed that EDV less than 25 cm/s was present in 11.1% of the patients with mild-to-moderate TBI [Glasgow Coma Score (GCS)>8] and in 46.7% of the patients with severe TBI (GCS≤8). PI more than 1.3 was present in 16.7% of the patients with GCS more than 8 and in 46.7% of the patients with GCS less than or equal to 8. The incidence of vasospasm was highest on the fifth day after trauma as it was detected in 16.7% of the patients with GCS more than 8 and in 40% of the patients with GCS less than or equal to 8. The logistic regression analysis of outcome predictors showed that the initial PI more than 1.3 had 91% sensitivity and 89% specificity and EDV less than 25 cm/s had 88% specificity and sensitivity 85% in predicting poor outcome; meanwhile, cerebral vasospasm had 84% sensitivity and 75% specificity in poor outcome prediction.
Conclusion Early abnormal CBF velocity detected by TCD following TBI can predict poor outcome at discharge from the hospital.

Keywords: neurologic outcome, transcranial Doppler, traumatic brain injury


How to cite this article:
Aly AA, Farmawy MS. Transcranial Doppler to detect early abnormalities in cerebral hemodynamics following traumatic brain injury in adult patients. Res Opin Anesth Intensive Care 2020;7:274-81

How to cite this URL:
Aly AA, Farmawy MS. Transcranial Doppler to detect early abnormalities in cerebral hemodynamics following traumatic brain injury in adult patients. Res Opin Anesth Intensive Care [serial online] 2020 [cited 2020 Oct 23];7:274-81. Available from: http://www.roaic.eg.net/text.asp?2020/7/3/274/296620


  Introduction Top


Morbidity and mortality after traumatic brain injury (TBI) depend on the primary brain damage as well as the extent of the secondary brain insult. The goal of management of patients with TBI should be focused on prevention and management of such secondary brain insult, which is caused mainly by imbalance between oxygen delivery and oxygen utilization of the brain tissue [1],[2]. Optimizing oxygen delivery to the brain in such patients requires close monitoring of cerebral blood flow (CBF) as well as intracranial pressure (ICP), which is not always applicable [3]. Transcranial Doppler (TCD) is a noninvasive bedside monitor that allows real-time, repeated measurement of CBF velocities by visualizing the intracranial vessels through acoustic windows, which is very important not only for diagnosis but also to guide the neurocritical care management [4],[5]. TCD can be used in TBI to diagnose cerebral vasospasm, hyperemia, changes in CBF velocities, and increased ICP [3],[6],[7]. Cerebral vasospasm, which is a common finding in TBI, can lead to secondary brain insult affecting the neurological outcome; however, it may go unrecognized [8],[9]. Changes in CBF velocities can be used to detect increased ICP with a correlation between the Gosling pulsatility index (PI) and ICP, making TCD a valuable noninvasive tool to identify patients who need invasive ICP monitoring [1],[3],[5]. Changes in CBF velocities following TBI are mostly pronounced in the early post-traumatic period and were suggested by some studies to correlate with patient outcome [10],[11]. We conducted this prospective observational study to screen for abnormalities in CBF in the early period following TBI using TCD. We also aimed at detecting the correlation between early changes in CBF velocity and early neurologic outcome.


  Patients and methods Top


The study was carried out in the Zagazig University Hospital Trauma and Surgical ICU after obtaining the hospital ethical committee approval during the time from August 2015 to December 2016. The relatives of the patients were provided with the detailed information about the research protocol, and written informed consents were obtained. The study included 66 adult patients (age>18 years) admitted to the ICU within 8 h of a diagnosis of TBI. Patients were excluded if they had poor ultrasound temporal acoustic window, any temporal lesion interfering with adequate TCD examination, and cardiovascular condition that may affect TCD measurements like significant arrhythmia or valvular stenosis. Patients were also excluded if they had polytrauma, organ failure, or history of cardiac arrest before admission. All patients were continuously monitored using a five-lead ECG, pulse oximetry, and invasive blood pressure through a radial artery catheter. Patients were managed according to the standardized local protocol of managing TBI aiming at optimizing cerebral perfusion and oxygenation. Mean arterial pressure was maintained around 90 mmHg and any decrease was managed using fluid boluses, vasopressor, or inotropic support as necessary to maintain cerebral perfusion pressure (CPP) more than 60 mmHg. Estimated ICP more than 20 mmHg was managed by sedation, intravenous mannitol 20% in a dose of 0.5 g/kg, through intermittent boluses with close monitoring of blood pressure. Adequate cerebral oxygenation was maintained by keeping SpO2 more than 95% and hemoglobin concentration more than 10 g/dl. Patients were kept normothermic and normoglycemic. Patient with severe TBI [Glasgow Coma Score (GCS≤8)] were intubated, sedated, and mechanically ventilated, maintaining normocapnia (PaCO2 between 35 and 40 mmHg).

After a period of resuscitation, TCD (Multi-Doppler, serial no. MDP0980; Siemens Acuson, Siemens Healthcare GmbH Henkestr, Erlangen, Germany) examination was done as soon as possible where two measurements were performed daily for the first 72 h, then once daily till 7 days after the TBI or discharge from ICU. TCD examination was also performed with any deterioration of the patient’s neurological condition assessed by GCS. Both right and left middle cerebral arteries (MCAs) were insonated using 2-MHz pulsed Doppler probe, which was placed over the temporal window just above the zygomatic arch to identify M1/M2 section of the MCA at a depth of 45–60 mm, and the angle of insonation was adjusted to give the best quality visual and acoustic signal. The internal carotid arteries (ICAs) were insonated in the upper cervical region using 4 MHz probe and choosing the depth and angle of insonation that provided the best signal. All TCD measurements were performed by experienced ICU staff members, and each patient was examined by the same examiner to minimize interobserver variability. Tracings of TCD were recorded for at least 10 cardiac cycles after 30 s of stabilization [4],[12],[13]. The end-diastolic velocity (EDV), peak systolic velocity (PSV), and mean flow velocity (mFV) in the MCA and the mean velocity in the extracranial ICA were recorded and then the worst value of the two sides was used for further calculation and analysis. The PSV is recognized as the first peak on TCD waveform on each cardiac cycle, the EDV is calculated from the point just before the next upstroke ([Figure 1]), and the mFV equals (PSV+2×EDV)/3. The PI was calculated as difference between the PSV and EDV divided by mFV in the MCA (PI=PSV−EDV/mFV) [14]. Lindegaard ratio (LR) was calculated as the ratio between the mFV in the MCA and extracranial ICA [9]. CPP was estimated using the formula reported by Schmidt et al. [15]: eCPP=MAP×EDV/mFV+14, and then ICP was estimated by subtracting CPP from MAP.
Figure 1 Transcranial Doppler flow velocity measurements of middle cerebral artery. EDV, end-diastolic velocity; PSV, peak systolic velocity.

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A PI more than 1.3 and an EDV less than 25 cm/s were considered abnormal, and cerebral vasospasm was diagnosed when the mFV in the MCA is more than 120 cm/s and LR is more than 3 [9],[16],[17].

The outcome of the patients was evaluated at discharge from the hospital using the Glasgow Outcome Scale (GOS) which ranges from 1 to 5 ([Table 1]), where scores 4 and 5 were considered as good outcome and scores 1–3 were considered as poor outcome. The observer who evaluated the GOS was unaware of the TCD measurements and the patient’s admission condition.
Table 1 Glasgow Outcome Scale [18]

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Data were analyzed using SPSS, version 20 (SPSS Inc., Chicago, Illinois, USA). Quantitative variables were expressed as mean±SD and analyzed using Student’s t-test whereas categorical data were expressed as number and percentage and analyzed using χ

2-test. Correlation between abnormal TCD findings and GOS was tested using Pearson’s correlation coefficient (r). Predictors of poor outcome were identified using univariate logistic regression. For all tests, P value less than 0.05 was considered significant.

The sample size was calculated based on previous studies on outcome prediction after TBI [5],[11] to give 80% power of calculation and 95% confidence interval using Open Epi (www.OpenEpi.com).


  Results Top


[Table 2] shows the demographic data and characteristics of the patients on admission. A total of 66 patients who had TBI were included in the study, including 42 males and 24 females, with a mean age of 32.48±14.5 years. Thirty-six (54.5%) patients had mild-to-moderate TBI with a GCS more than 8, whereas 30 (45.5%) patients had severe TBI with a GCS less than or equal to 8. The mean time between admission and first TCD examination was 48±18 min.
Table 2 Patient’s demographic data and admission characteristics

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The patients were divided into two groups according to their GCS on admission, and the comparison of the TCD findings. [Table 3] showed that EDV was significantly higher in patients with GCS > 8 than in patients with GCS ≤ 8 to 8 (37.8±14.2 vs. 22.5±9.4, P<0.05). The PI was significantly lower in patients with GCS > 8 than in patients with GCS ≤ 8 (1.02±0.34 vs. 1.76±0.38, P<0.05). LR on admission was nonsignificantly lower in patients with GCS > 8 than in patients with GCS ≤ 8 (1.45±0.66 vs. 2.14±0.84).
Table 3 Comparison of the initial transcranial Doppler data and Glasgow Outcome Scale in patients with Glasgow Coma Score more than 8 and patients with Glasgow Coma Score less than or equal to 8

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The mean first 72-h TCD findings of the patients showed an increase in flow velocities in both groups. The LR was significantly lower in patients with GCS more than 8 than in patients with GCS less than or equal to 8 (1.62±0.46 vs. 2.58±0.82 P<0.05). The calculated ICP was significantly lower in patients with mild-to-moderate TBI than in patients with severe TBI (18±7 vs. 26±11, P<0.05).

The outcome of the patients evaluated by GOS revealed that eight (22.2%) patients had poor outcome (two deaths, two vegetative state, and four severe neurologic disability) and 28 (77.8%) patients had good outcome (12 had moderate disability and 16 had good recovery) in the group with GCS more than 8. In contrast, 18 (60%) patients had poor outcome (four deaths, eight vegetative state, and six severe neurologic disability) and 12 (40%) patients had good outcome (eight had moderate disability and four had good recovery) in the group with GCS less than or equal to 8. The difference between the two groups was significant (P<0.05). The length of hospital stay was significantly shorter in patients with GCS > 8 than in patients with GCS ≤ 8 (13.2±7.7 vs. 24.2 ±9.2 days, P<0.05).

[Figure 2] shows the number of patients who had abnormal TCD findings on admission. The patients who had a EDV less than 25 cm/s were four (11.1%) among those with GCS > 8 and among 14 (46.7%) patients with GCS ≤ 8, and the difference between the two groups was significant. PI more than 1.3 was present in six (16.7%) patients with GCS > 8 and in 14 (46.7%) patients with GCS ≤ 8, and the difference between the two groups was significant (P<0.05). In our study, all the patients who had EDV less than 25 cm/s also had PI more than 1.3 in the group with GCS ≤ 8, whereas only four of the six patients with EDV less than 25 cm/s also had PI more than 1.3 in the group with GCS more than 8. LR more than 3 was not detected in any patient with GCS > 8 on admission but was present in four (13.3%) patients with GCS ≤ 8, and the difference was nonsignificant (P>0.05).
Figure 2 Number of patients with abnormal transcranial Doppler findings on admission in patients with GCS more than 8 (filled columns) and patients with GCS less than or equal to 8 (open columns). EDV, end-diastolic velocity; GCS, Glasgow Coma Scale; LR, Lindegaard ratio; PI, pulsatility index. *P is significant between the two groups.

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[Figure 3] shows the incidence of cerebral vasospasm during the 7 days following trauma. On the first day of trauma, vasospasm was not detected in any patient with GCS more than 8, but detected in two (6.7%) patients in the group with GCS ≤ 8. On the second day of trauma, vasospasm was detected in two (5.5%) patients in the group with GCS > 8 and in four (13.3%) patients in the group with GCS less than or equal to 8. On the third day of trauma, four (11.1%) patients with GCS > 8 and eight (26.6%) patients with GCS ≤ 8 had cerebral vasospasm, and the difference between the two groups was significant (P<0.05). On the fourth day after trauma, cerebral vasospasm was still present in four (11.1%) patients with GCS > 8 and in 12 (40%) patients with GCS ≤ 8, and the difference was significant (P<0.05). Six (16.7%) patients with GCS > 8 and 12 (40%) patients with GCS ≤ 8 still had vasospasm on the fifth day following trauma, and the difference between the two groups was significant (P<0.05). Six days after the trauma, vasospasm was present in four patients with GCS > 8 and in eight patients with GCS ≤ 8. On the seventh day after trauma, four (11.1%) patients with GCS > 8 and six (20%) patients with GCS ≤ 8 still had cerebral vasospasm.
Figure 3 Number of patients diagnosed by transcranial Doppler as having cerebral vasospasm during the first 5 days after trauma, *P is significant between patients with GCS more than 8 (filled columns) and patients with GCS less than or equal to 8 (open columns). GCS, Glasgow Coma Scale.

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The admission GCS had a significant positive correlation with GOS (r=0.48, P<0.05). The initial EDV had a significant positive correlation with the GOS (r=0.52, P<0.01). The initial PI had a significant negative correlation with the GOS (r=−0.55, P<0.01). The initial mFV and LR did not have a significant correlation with the GOS (P>0.05), as shown in [Table 4].
Table 4 Correlation of Glasgow Outcome Score with Glasgow Coma Score and transcranial Doppler data on admission

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The logistic regression analysis of poor outcome predictors. [Table 5] showed that PI more than 1.3 on admission had the highest diagnostic accuracy (94%) in predicting poor outcome with 91% sensitivity and 89% specificity. Diastolic flow velocity (dFV) less than 25 cm/s also had high accuracy (84%) in predicting poor outcome with 88% sensitivity and 85% specificity. Admission GCS had 75% accuracy, 80% sensitivity, and 72% specificity in predicting poor outcome. In contrast, vasospasm had 79% accuracy, 84% sensitivity, and 75% specificity in poor outcome prediction.
Table 5 Logistic regression analysis of poor outcome (Glasgow Outcome Scale 1–3) predictors

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  Discussion Top


The results of this study revealed that patients with severe TBI (GCS≤8) had a significantly lower EDV and higher PI than patients with mild-to-moderate TBI (GCS>8). Patients with severe TBI also had higher incidence of vasospasm than patients with mild-to-moderate TBI. The TCD findings of the study also showed that lower admission GCS, lower EDV, and higher PI significantly correlated with poor early neurologic outcome of the patients. PI more than 1.3 and EDV less than 25 cm/s on admission had the highest sensitivity and specificity in predicting poor outcome.

TCD bedside availability makes it a useful tool in detecting the flow velocity changes, which occurs in the early post-traumatic period. These changes include low flow state especially in the first 8 hours after trauma and subsequent vasospasm or hyperemia [6],[19]. Low EDV associated with high PI has been proposed as the most reliable TCD parameter to detect cerebral hypoperfusion, where a small decrease in EDV and PI reflects an increase in downstream vascular resistance and hence decrease in CPP even after mild-to-moderate TBI [5],[20].

In this study, the initial TCD findings showed that, patients with severe TBI had significantly lower EDV and higher PI than patients with mild-to-moderate TBI. Han et al. [20] studied 121 patients with mild to severe TBI and reported that admission CBF velocities were related to GCS with lower flow velocities in patients with severe TBI. Van Santbrink et al. [10] also reported that the low flow velocity after TBI correlated with the severity of injury and neurologic outcome.

Ract et al. [5] studied 24 patients with severe TBI and reported that 46% of the patients had abnormal TCD findings on admission, but they considered TCD abnormal if the patient had two of the following three parameters: mFV less than 30 cm/s, EDV less than 20 cm/s, and PI more than 1.4. In contrast, Bouzat et al. [21] studied 356 patients with mild-to-moderate TBI and reported abnormal TCD findings in 24.4% of the patients on admission, considering TCD abnormal if the patient had EDV less than 25 cm/s or PI more than 1.25. In our study, 16.7% of the patients with mild-to-moderate TBI and 46.7% of the patients with severe TBI had abnormal TCD on admission using the values of EDV less than 25 cm/s or PI more than 1.3 to define abnormal TCD.

The TCD results of this study revealed that cerebral vasospasm was most prevalent on the fifth day after trauma, reaching 16.7% in patients with mild-to-moderate TBI and 40% in patients with severe TBI. On all 7 days of TCD recording, more patients with severe TBI had vasospasm than patients with mild-to-moderate TBI, especially on the third, fourth, fifth, and sixth day after trauma, where the difference was significant. Those results are in accordance with the previous studies confirming the severity of the TBI as a risk factor for the development of cerebral vasospasm [22],[23]. Post-traumatic vasospasm has been reported to start most frequently on the second day after trauma; however, maximal flow velocities are observed between the third and fifth day and tend to last for 5–15 days [24],[25],[26]. The incidence of vasospasm after TBI varies among literatures from 35 to 61% with higher incidence and longer duration if the vasospasm is associated with traumatic subarachnoid hemorrhage [22],[24],[25],[27],[28].

This study showed that among patients with mild-to-moderate TBI (GCS>8), 28 (77.8%) patients had good early neurologic outcome but eight (22.2%) patients had poor outcome. Bouzat et al. [21] studied the early neurologic outcome (28 days after trauma) of 356 patients with mild and moderate TBI and reported that 69% of the patients had good outcome and 31% of them had poor outcome.

Our results also revealed that 12 (40%) patients with severe TBI had good early neurologic outcome and 18 (60%) patients had poor outcome. Those results are close to the results of two previous studies done by van Santbrink et al. [10] and von Elm et al. [29], who assessed the GOS of patients with severe TBI 3 months after the trauma and reported poor outcome in 56 and 59% of the patients, respectively. In contrast, Ract et al. [5] studied 24 patients with severe TBI and reported that only 30% of the patients had poor outcome 3 months after the injury, and the difference in incidence among literature may be due to different timing of outcome evaluation.

The results of our study showed that on admission to the ICU, lower GCS, lower dVF, and higher PI were significantly correlated with poor early neurologic outcome. PI more than more than 1.3 followed by dVF less than 25 cm/s had the highest accuracy in predicting the poor outcome (94 and 84%, respectively). Jaffres et al. [30] reported that high PI was the TCD parameter associated with neurologic worsening after mild-to-moderate TBI. Bouzat et al. [17] reported that PI more than 1.25 and EDV less than 25 cm/s had high sensitivity and specificity in predicting neurologic worsening 7 days after mild-to-moderate TBI. Similar results were also reported in two studies done on patients with severe TBI where PI more than 1.3 and EDV less than 25 cm/s were predictive of poor outcome [5],[31]. Being dimensionless and independent of sampling technique, high PI has been reported to be the TCD parameter that can define low flow velocity confirming that low velocities are owing to actual increase in pulse amplitude, whereas normal PI even in the presence of low flow velocity values is probably indicative of wide angle of insonation [5],[32]

The GCS less than or equal to 8 on admission had 80% sensitivity and 72% specificity in predicting early poor neurologic outcome after TBI. The results of different literature studies on the value of GCS in outcome prediction are conflicting. In two studies on mild TBI, GCS was found to have only modest ability to predict outcome, but the two studies used a different neuropsychiatric score other than GOS to predict outcome [33],[34]. Van Santbrink et al. [10] considered the initial GCS as a strong covariant to low flow velocity in predicting poor outcome after severe TBI; however, Ract et al. [5] found no correlation between admission GCS and 3-month GOS. This discrepancy may be explained by the change that can occur in GCS owing to either secondary brain injury or neurologic recovery.

Berry et al. [8] and Armonda et al. [24] have reported post-traumatic cerebral vasospasm as a predictor of poor neurological outcome when associated with low CBF, which is in accordance with our results, where vasospasm had 79% accuracy (84% sensitivity and 75% specificity) in predicting poor outcome.

A possible limitation of this study is the early prediction of outcome at discharge as neurologic recovery may still occur. Another limitation is the intermittent TCD monitoring.

From the results of this study, we can conclude that abnormal cerebral flow velocities detected by TCD on admission were more prevalent in patients with severe TBI than in patients with mild-to-moderate TBI. The results also revealed that the admission EDV less than 25 cm/s and PI more than 1.3 had high sensitivity and specificity in predicting poor outcome at hospital discharge, whereas admission GCS less than or equal to 8 and cerebral vasospasm were also predictors of poor outcome with less sensitivity and specificity. Therefore, TCD can be very useful to detect early abnormal cerebral flow velocities following TBI; thus, identifying patients at risk of poor outcome can guide the management of such patients, thus preventing secondary brain insult and poor neurologic outcome.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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Abstract
Introduction
Patients and methods
Results
Discussion
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