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 Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 6  |  Issue : 2  |  Page : 200-205

Assessment of brain midline shift using sonography in neurocritical patients


Department of Critical Care Medicine, Faculty of Medicine, University of Alexandria, Alexandria, Egypt

Date of Submission04-Jun-2018
Date of Acceptance05-Feb-2019
Date of Web Publication12-Jun-2019

Correspondence Address:
Tamer A Helmy
Professor in Department of Critical Care Medicine, Alexandria university, Alexandria
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/roaic.roaic_47_18

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  Abstract 

Introduction Brain midline shift (MLS) is a life-threatening condition that requires urgent diagnosis and treatment.
Aim of the work The aim of this study was to assess the brain MLS using transcranial sonography (TCS) and compare it with that of plain computed tomography (CT) in neurocritical patients.
Patients and methods The study was carried out on 50 neurocritical patients admitted to the Alexandria Main University Hospitals at the Critical Care Medicine Units with a Glasgow coma score of less than 8. The ultrasound (US) MLS was measured through the temporal bone window by measuring the difference between the distance from the skull to the third ventricle on both sides as soon as possible before obtaining the brain CT. CT MLS was determined by measuring either the difference between the distance from the external bone table and the center of the third ventricle bilaterally (method 1) or the distance between the ideal midline and the septum pellucidum (method 2).
Results A total of 50 neurocritical patients were included. The MLS (mean±SD) was 4.18±2.15 mm using US and 5.06±2.47 mm using CT (method 1) and 5.23±2.60 mm using CT (method 2). The Pearson’s correlation coefficient (r) between US MLS and CT MLS was 0.986 with method 1 (P<0.001) and 0.984 with method 2 (P<0.001). The area under the receiver operating characteristic curve for detecting a significant MLS with TCS was 0.990 (95% confidence interval=0.916–1.000%) in (method 1) and, using 4 mm as a cutoff, the sensitivity was 94.7%, the specificity 93.5%, and the positive predictive value was 90% and the negative predictive value was 96.7%. The area under the receiver operating characteristic curve for detecting a significant MLS with TCS was 0.988 (95% confidence interval=0.916–1.000%) (in method 2) and, with a cutoff of 4 mm, the sensitivity was 95% %, the specificity was 96.6%, and the positive predictive value was 95% and the negative predictive value was 96.7%.
Conclusion This study suggests that TCS could detect MLS with reasonable accuracy in neurocritical patients and that could serve as a bedside tool to facilitate early diagnosis and treatment for patients with a significant intracranial mass effect.

Keywords: brain computed tomography, brain midline shift, transcranial sonography


How to cite this article:
Helmy TA, Abdelhady MA, Ahmed HA. Assessment of brain midline shift using sonography in neurocritical patients. Res Opin Anesth Intensive Care 2019;6:200-5

How to cite this URL:
Helmy TA, Abdelhady MA, Ahmed HA. Assessment of brain midline shift using sonography in neurocritical patients. Res Opin Anesth Intensive Care [serial online] 2019 [cited 2019 Oct 14];6:200-5. Available from: http://www.roaic.eg.net/text.asp?2019/6/2/200/260147


  Introduction Top


In neurocritical care, one of the most life-threatening conditions that require urgent intervention is brain midline shift (MLS). In addition to the clinical examination, computed tomography (CT) is considered to be the cornerstone technique for management of those patients [1].

A CT scan classification based on data from the Traumatic Coma Data Bank was proposed by Marshall and colleagues, including an MLS of more than 0.5 cm as one of the main criteria for the severity of traumatic brain injury [2],[3].

Ropper observed that following stroke, alteration of consciousness was directly proportional to the MLS on CT [4] and Pullicino et al. [5] found that both MLS and coma were independent predictors of mortality at 15 days following acute stroke.

Early detection of MLS is thus very important because it allows the implementation of an appropriate treatment plan (North American recommendations from 2006 call for a surgical evacuation in the case of an MLS > 0.5 cm in the presence of severe traumatic brain injury, extradural, subdural, or intracerebral hematoma) [6].

However, even though head CT is considered to be the gold standard technique to diagnose MLS, serial CTs of ICU patients can be associated with significant morbidity and secondary brain injuries related to their transport [7]. Routinely repeated CT scans, even in patients with significant brain injuries, does not contribute to patient care [8].

Transcranial B-mode sonography (TCS) is a neuroimaging technique that displays the brain parenchyma and the intracranial ventricular system through the intact skull. Seidel and colleagues described in 1996 a simple method to determine the MLS with sonography. This study evaluated the dislocation of the third ventricle from the brain midline by transcranial duplex sonography in 10 healthy volunteers. The mean dislocation was 0.2±0.3 mm. Eighteen stroke patients were investigated within 12 h by both duplex sonography and CT and the dislocation of the third ventricle was measured. Correlation between the two methods was high (r=0.87). This seemed to correlate well with CT findings. In addition, it could be an early outcome predictor by rapidly detecting a significant MLS in acute stroke [9].


  Aim of the work Top


The aim of this study was to assess the brain MLS using TCS and compare it with that of plain CT in neurocritical patients.


  Patients and methods Top


This prospective study was carried out on 50 neurocritical adults of both sexes (according to sample size calculation using G power) who were admitted to the Alexandria Main University Hospitals at the Critical Care Medicine Department. Approval of the medical ethics committee of Alexandria Faculty of Medicine and an informed consent was taken from the patient or the next of kin before conducting the study.

Inclusion criteria

  1. Neurocritical patients with Glasgow coma score (GCS) of less than 8.
  2. Patients of age more than 18 years.


Exclusion criteria

  1. Decompressive craniectomy.
  2. Patients with temporal subcutaneous hematoma.
  3. Maxillofacial trauma.


All patients included in the study were subjected to complete history taking, systematic clinical examination, and full neurological assessment. GCS was calculated on admission.

The ultrasound (US) MLS was measured through the temporal acoustic bone window using a low frequency (2–4 MHz) probe using (EMP 2100) an US device prior to plain brain CT. The third ventricle was identified as a double hyperechogenic image over the midbrain; the distance between the external bone table and the center of the third ventricle was measured bilaterally in millimeters and the difference between the two readings divided by two was used to calculate the MLS.

The CT MLS was measured by two methods:

The distance between the external bone table and the center of the third ventricle at the orbitomeatal plane, allowing visualization of the third ventricle (in the same plane as the sonographic measurement) [10].

The distance between the ideal midline and the septum pellucidum [11].

CT method (1) was used as a gold standard and 5 mm was considered a significant MLS.

The measurement of MLS using TCS was compared with that of plain CT.

Statistical analysis of the data

Data were fed to the computer and analyzed using IBM SPSS software package, version 20.0 (IBM, USA). Qualitative data were described using number and percent. Quantitative data were described using range (minimum and maximum), mean, SD, and median. Significance of the obtained results was judged at the 5% level.

The used tests were

  • Paired t test: for normally quantitative variables, to compare between two periods.
  • Pearson’s coefficient: to correlate between two normally quantitative variables.
  • Kruskal–Wallis test: for abnormally quantitative variables, to compare between more than two studied groups.
  • Spearman’s coefficient: to correlate between two abnormally quantitative variables.
  • Receiver operating characteristic (ROC) curve: it is generated by plotting sensitivity (TP) on the y axis versus 1-specificity (FP) on the x axis at different cutoff values. The area under the ROC curve denotes the diagnostic performance of the test. Area more than 50% gives acceptable performance and area about 100% is the best performance for the test. The ROC curve allows also a comparison of performance between two tests.
  • Bland and Altman plot: for the agreement between two quantitative values.



  Results Top


Sixty percent of the studied patients were men. The mean age was 48.90±21.19 years. The mean admission GCS was 7.12±1.66. All the cases were mechanically ventilated. Twenty-one (42%) patients of the studied cases died, the length of ICU stays ranged from 1 to 24 days with a mean of 11.04±6.30. The days on mechanical ventilator ranged from 1 to 24 days, mean±SD 7.36±7.02 ([Table 1]).
Table 1 Distribution of the studied cases according to Marshall classification (N=50)

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Computed tomography results

CT MLS was 5.06±2.47 mm (using method 1) and 5.23±2.60 mm (using method 2). An MLS of more than 5 mm with CT was observed in 17 (34%) patients.

Transcranial sonography results

Measurement of MLS by TCS showed an average of 4.18±2.15 mm. An MLS of more than 5 mm was observed in 12 (24%) patients. The correlation coefficient between US MLS and CT MLS was 0.986 with method 1 (P <0.001), and 0.984 with method 2 (P<0.001).

The correlation coefficient between CT MLS (method 1) and CT MLS (method 2) was 0.995 (P<0.001). The limits of agreements for MLS measurements with US and the two CT methods are presented in [Table 2], showing a bias of −0.88 mm and limits of agreement from −1.02 to −0.74 mm for US and CT (method 1) and a bias of −1.05 mm and limits of agreement from −1.23 to −0.88 mm for US and CT (method 2).
Table 2 Agreement of ultrasound with computed tomography methods 1 and 2

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The sensitivity and the specificity of US to detect a significant MLS (i.e. MLS >5 mm) were analyzed with the ROC curve. In method (2) the area under the ROC curve was 0.988 (95% confidence interval=0.916–1.000%) and with a cutoff of 4 mm, the sensitivity was 95%, the specificity 96.6%, and the positive predictive value was 95% and the negative predictive value was 96.7%.

When the CT (method 1) was used to define a ‘significant’ MLS (i.e. MLS >5 mm), the area under the ROC curve was 0.990 and with a cutoff of 4 mm, the sensitivity was 94.7%, and the specificity was 93.5%. The positive predictive value was 90% and the negative predictive value was 96.7%.

The bias between both methods (method 1 and method 2) was −0.146 mm, and the correlation coefficient was 0.995 (P<0.001) ([Figure 1]).
Figure 1 ROC curve forthe detection of a CT MLS (method 1)>5 mm (with TCS.CT computed tomography; MLS; midline shift TCS, transcranial sonography.

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The correlation coefficient of the difference between US MLS and CT MLS was 0.641 (P<0.001). The smaller the MLS the narrower the difference between the measurement of US MLS and CT MLS.

The narrowest difference between US MLS and CT MLS (0.37±0.12) was observed at an MLS of less than 2 mm.

Twenty-one (42%) patients of the studied cases died; the length of ICU stays ranged from 1 to 24 days with a mean of 11.04±6.30. The days of mechanical ventilator ranged from 1 to 24 days (mean, 7.36±7.02).

There was significant relation between US MLS and mortality; 100% of the cases survived with a US MLS of less than 4 mm. Eighty-three percent died when the US MLS was (4–6 mm;100% of the cases with a US MLS greater than 6 mm died ([Table 3],[Table 4],[Table 5]).
Table 3 Relation between computed tomography midline shift and (difference between ultrasound midline shift and computed tomography midline shift)

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Table 4 Correlation between ultrasound midline shift with Glasgow coma score, ICU stay, and ventilation days

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Table 5 Relation between ultrasound midline shift with Glasgow coma score, ICU stay, and ventilation days

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The relation between US MLS and GCS was statistically significant, the greater the US MLS the lower the GCS. The relation between US MLS and length of ICU stay and ventilation days was tested and it was statistically significant. The greater the US MLS the longer the length of ICU stay and ventilation days, except in patients with an US MLS of greater than 6 mm because of early death.


  Discussion Top


The early detection of an MLS in neurosurgical patients is very important because it allows the implementation of an appropriate treatment plan. Brain CT is considered to be the gold standard to diagnose MLS. Serial CTs in neurosurgical ICU patients can be associated with significant morbidity and secondary brain injuries related to their transport.

Our study suggested that it is possible to detect MLS with a reasonable accuracy in neurocritical patients with various intracranial pathologies using TCS. This could facilitate early diagnosis and treatment for patients with significant intracranial mass effects. It is a noninvasive tool, decreases exposure to radiation, and hazards of transport.

Bogdahn et al. [12] described for the first time the identification of cerebral structures with sonography and was able to identify the third ventricle in 45 of 52 patients.

Seidel et al. [9] subsequently proposed to measure the MLS with US by setting the center of the third ventricle as a reference. This method was used to determine the mass effect of patients presenting with acute ischemic stroke [9].Gerriets et al. [13] studied the value of MLS measurement to predict fatal outcome at different time points after stroke onset. It showed that an US MLS of more than 4 mm within the first 32 h was associated with a near 100% mortality, with the exception of a patient having undergone decompressive craniectomy [13].

Transcranial duplex sonography was used to monitor ventricular width in patients with hydrocephalus. Ninety-two attempts to clamp either lumbar or extraventricular drainage were monitored in 37 patients during a 1-year period. A cutoff value for increase of ventricular width of 5.5 mm yielded high sensitivity (100%) and specificity (83%) [14].

In 61 patients with supratentorial ischemic infarction, the sonographic measurement of MLS was compared with cranial CT in a 12-h time window. Transcranial color-coded duplex sonography and cranial CT measurements of MLS were correlated, the correlation coefficient was more than 0.9 [15].

Motuel et al. [16] tested the accuracy of sonography in detecting MLS in comparison with CT, 52 neurosurgical ICU patients were included. The Pearson’s correlation coefficient (r) between sonography and CT scan was 0.65 (P<0.001). The sensitivity was 84.2% and the specificity was 84.8%.

In our study, the best correlation between TCS and CT was obtained by using the distance between the external bone table and the center of the third ventricle measured from the CT cuts in the orbitomeatal plane that allowed visualizing the third ventricle (method 1), with a bias of only −0.88 mm. The correlation coefficient between TCS and CT was slightly better when using CT method 1 compared with method 2 (0.986 vs. 0.984). The bias was smaller and the limits of agreement were narrower when using CT method 1 (mean bias of −0.88 mm and limits of agreement from −1.02 to −0.74 mm) for TCS and CT method 1 versus a mean bias of −1.05 mm and limits of agreement from −1.23 to −0.88 mm for TCS and CT method 2. This could be due to the fact that CT method 1 uses the same imaging plane as TCS, whereas CT method 2 uses a different plane (which is the neuroradiologists’ conventional way to measure MLS). Using a different imaging plane could, thus, have increased the bias between sonography and CT without affecting the correlation.

In our study, we found that TCS seemed to systematically underestimate the CT MLS (the MLS was 4.18±2.15 mm with TCS, 5.06±2.47 mm with CT method 1, and 5.23±2.60 mm with CT method 2).

In our study, the ability to detect significant MLS (>5 mm in CT scan) with TCS was good, with a sensitivity and specificity of around 95% when using a threshold for a significant MLS set at 4 mm, although MLS was underestimated by TCS. The smaller the MLS the narrower the difference between the measurement of US MLS and CT MLS.

The relation between US MLS and GCS was statistically significant, the greater the US MLS the lower the GCS. The relation between US MLS and length of ICU stay and ventilation days was tested and it was statistically significant. The greater the US MLS, the longer the length of ICU stay and ventilation days, except in patients with an US MLS of greater than 6 mm because of early death.


  Conclusion Top


This study suggests that TCS could detect MLS with reasonable accuracy in neurocritical patients and may serve as a reliable bedside tool to facilitate early diagnosis and treatment for patients with a significant intracranial mass effect.

Study limitations

The measurement of MLS using sonography and CT were not simultaneous and as the brain MLS can change rapidly, it is possible that the decrease in agreement between methods could in part be due to the changing MLS at different time points.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

1.
Marshall LF, Marshall SB, Klauber MR, Van Berkum CM, Eisenberg H, Jane JA et al. The diagnosis of head injury requires a classification based on computed axial tomography. J Neurotrauma 1992; 9:287–292.  Back to cited text no. 1
    
2.
Marshall LF, Marshall SB, van Berkum CM, Eisenberg HM, Jane JA, Luerssen TG et al. A new classification of head injury based on computerized tomography. J Neurosurg 1991; 75:14–20.  Back to cited text no. 2
    
3.
Maas AI, Hukkelhoven CW, Marshall LF, Steyerberg EW. Prediction of outcome in traumatic brain injury with computed tomographic characteristics: a comparison between the computed tomographic classification and combinations of computed tomographic predictors. Neurosurgery 2005; 57:1173–1182.  Back to cited text no. 3
    
4.
Ropper AH. Lateral displacement of the brain and level of consciousness in patients with an acute hemispheral mass. N Engl J Med 1986; 314:953–958.  Back to cited text no. 4
    
5.
Pullicino PM, Alexandrov AV, Shelton JA, Alexandrova NA, Smurawska LT, Norris JW. Mass effect and death from severe acute stroke. Neurology 1997; 49:1090–1095.  Back to cited text no. 5
    
6.
Bullock MR, Chesnut R, Ghajar J, Gordon D, Hartl R, Newell DW et al. Surgical management of traumatic parenchymal lesions. Neurosurgery 2006; 58:S25–S46.  Back to cited text no. 6
    
7.
Andrews PJ, Piper IR, Dearden NM, Miller JD. Secondary insults during intrahospital transport of head-injured patients. Lancet 1990; 335:327–330.  Back to cited text no. 7
    
8.
Kaups KL, Davis JW, Parks SN. Routinely repeated computed tomography after blunt head trauma: does it benefit patients? J Trauma 2004; 56:475–480.  Back to cited text no. 8
    
9.
Seidel G, Gerriets T, Kaps M, Missler U. Dislocation of the third ventricle due to space-occupying stroke evaluated by transcranial duplex sonography. J Neuroimaging 1996; 6:227–230.  Back to cited text no. 9
    
10.
Llompart P, Abadal C, Palmer M, Perez J, Casares M, Homar J et al. Monitoring midline shift by transcranial color-coded sonography in traumatic brain injury. A comparison with cranial computerized tomography. Intensive Care Med 2004; 30:1672–1675.  Back to cited text no. 10
    
11.
Foundation TBT. The American Association of Neurological Surgeons. The Joint Section on Neurotrauma and Critical Care. Computed tomography scan features. J Neurotrauma 2000; 17:597–627.  Back to cited text no. 11
    
12.
Bogdahn U, Becker G, Winkler J, Greiner K, Perez J, Meurers B. Transcranial color-coded real-time sonography in adults. Stroke 1990; 21:1680–1688.  Back to cited text no. 12
    
13.
Gerriets T, Stolz E, Modrau B, Fiss I, Seidel G, Kaps M. Sonographic monitoring of midline shift in hemispheric infarctions. Neurology 1999; 52:45–49.  Back to cited text no. 13
    
14.
Kiphuth IC, Huttner HB, Struffert T, Schwab S, Köhrmann M. Sonographic monitoring of ventricle enlargement in posthemorrhagic hydrocephalus. Neurology 2011; 76:858–862.  Back to cited text no. 14
    
15.
Stolz E, Gerriets T, Fiss I, Babacan SS, Seidel G, Kaps M. Comparison of transcranial color-coded duplex sonography and cranial CT measurements for determining third ventricle midline shift in space-occupying stroke. Am J Neuroradiol 1999; 20:1567–1571.  Back to cited text no. 15
    
16.
Motuel J, Biette I, Srairi M, Mrozek S, Kurrek MM, Chaynes P et al. Assessment of brain midline shift using sonography in neurosurgical ICU patients. Crit Care 2014; 18:676.  Back to cited text no. 16
    


    Figures

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    Tables

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



 

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