Correlation between optic nerve sheath diameter measured on imaging with acute pathologies found on computed tomography of trauma patients

Correlation between optic nerve sheath diameter measured on imaging with acute pathologies found on computed tomography of trauma patients

European Journal of Radiology 125 (2020) 108875 Contents lists available at ScienceDirect European Journal of Radiology journal homepage: www.elsevi...

2MB Sizes 0 Downloads 29 Views

European Journal of Radiology 125 (2020) 108875

Contents lists available at ScienceDirect

European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad

Correlation between optic nerve sheath diameter measured on imaging with acute pathologies found on computed tomography of trauma patients

T

Pinporn Jenjitrananta, Padcha Tunlayadechanonta, Thidathit Prachanukoolb, Rathachai Kaewlaia,1,* a b

Department of Diagnostic and Therapeutic Radiology, Ramathibodi Hospital, Mahidol University, Bangkok, Thailand Department of Emergency Medicine, Ramathibodi Hospital, Mahidol University, Bangkok, Thailand

A R T I C LE I N FO

A B S T R A C T

Keywords: Optic nerve sheath diameter Increased intracranial pressure Trauma patient CT US

Purpose: To evaluate the correlation between optic nerve sheath diameter (ONSD) measurement with signs of increased intracranial pressure (ICP) found on computed tomography (CT) in trauma patients. Materials and methods: 271 consecutive head CT trauma scans performed at our trauma center were retrospectively reviewed for ONSD and CT findings. Measurement of ONSD was made at CT and, when available, with ultrasonography (US). Imaging signs of increased ICP were assessed. Association between ONSD and signs of ICP were analyzed. Results: The mean ONSD on axial CT images, optic-nerve axial plane and US was 4.70 ± 0.59 mm, 4.78 ± 0.59 mm, and 3.16 ± 0.50 mm, respectively. The ONSD measured at CT was significantly higher than that measured by US(p < 0.01). No difference of ONSD measured at CT between axial and optic-nerve axial planes. Patients with CT evidence of increased ICP had significantly higher ONSD than those without imaging abnormalities (p = 0.0001-0.0064). The ONSD cutoff points for suggesting increased ICP were 4.8 mm (60.5 % sensitivity, 61.2 % specificity, 20.4 % PPV, 90.4 % NPV) at CT and 3.15 mm (97.4 % sensitivity, 13.8 % specificity, 15.7 % PPV, 97 % NPV) at US. Conclusion: There was a significant association between ONSD and imaging signs of increased ICP in CT with a high NPV. No difference of ONSD measurement at CT between normal and optic-nerve axial planes was observed, whereas there was a significant difference between diameter obtained at CT and US.

1. Introduction Increased intracranial pressure (ICP) is a serious complication found among patients with traumatic brain injury, particularly those in intensive care units. It is associated with poor outcome after traumatic brain injury (TBI) [1–3], may lead to brainstem injury [4] and potential deaths. Early detection and prompt management may prevent further brain damage and brain death [5]. There are several methods used to diagnose increased ICP [6]. While direct measurement using ventricular catheters or intraparenchymal ICP monitoring devices is the gold standard, they are invasive and may cause serious complications. Therefore, non-invasive methods have been proposed.

In recent years, several authors have examined the role of ultrasonography (US) for early detection of increased ICP by measuring the optic nerve sheath diameter (ONSD) [1,5–15]. Because the optic nerve sheath connects with intracranial subarachnoid space, its diameter is influenced by cerebrospinal fluid (CSF) pressure variation [16–19]. ONSD measurement is non-invasive and reasonably accurate, even when it was used by relatively inexperienced operators [20,21]. ONSD has been reported to be highly specific and highly sensitive (100 % and 95 %, respectively) for diagnosis of increased ICP [1,14,22]. In addition to US, other cross-sectional imaging modalities such as computed tomography (CT) and magnetic resonance imaging (MRI) can be used for ONSD measurement and at the same time provide direct

Abbreviations: ONSD, optic nerve sheath diameter; ICP, increased intracranial pressure; CT, computed tomography; US, ultrasonography; MRI, magnetic resonance imaging ⁎ Corresponding author at: Division of Emergency Radiology, Department of Diagnostic and Therapeutic Radiology, Ramathibodi Hospital, Mahidol University, 270 Rama VI Road, Ratchatewi, Bangkok 10400 Thailand. E-mail addresses: [email protected] (P. Jenjitranant), [email protected] (P. Tunlayadechanont), [email protected] (T. Prachanukool), [email protected] (R. Kaewlai). 1 Current address: Department of Radiology, Faculty of Medicine Siriraj Hospital, Mahidol University, 2 Wanglang Road, Bangkok Noi, Bangkok, 10700, Thailand. https://doi.org/10.1016/j.ejrad.2020.108875 Received 30 September 2019; Received in revised form 21 January 2020; Accepted 6 February 2020 0720-048X/ © 2020 Elsevier B.V. All rights reserved.

European Journal of Radiology 125 (2020) 108875

P. Jenjitranant, et al.

CT reports were reviewed by one of the investigators for intracranial hemorrhage, diffuse sulcal effacement, effacement of basal cistern, hydrocephalus, midline shift, brain herniation and bone fracture. For the purpose of statistical evaluation, when at least one of these findings except for bone fracture were present, the patient was deemed to have increased ICP. Intracranial hemorrhages were further classified into intraventricular hemorrhage (IVH), intraparenchymal hemorrhage (IPH), subdural hematoma (SDH), subarachnoid hemorrhage (SAH) and epidural hematoma (EDH).

evidence of increased ICP such as intracranial hemorrhage, effacement of basal cistern, diffuse sulcal effacement, midline shift, brain herniation and hydrocephalus [6,14,15,22–24]. However, their value may be overlooked because of limited research data [5,25,26]. There are very few investigations directly compare ONSD measurements obtained by different imaging techniques (i.e. US, CT and MRI) [26–28]. Appropriate imaging plane for ONSD measurement is also unclear. The primary purpose of this study was to evaluate the correlation of ONSD measurement with signs of increased ICP found at CT in traumatic brain injury (TBI) patients. The secondary purpose was to compare ONSD measurements obtained from US and CT in the same individuals.

2.3.2. US assessment All US studies were performed by 12 physicians (3 emergency radiologists and 9 emergency medicine residents) trained in ONSD measurement, who were on roster when patients arrived. All 9 emergency medicine residents had been trained and performed at least 25 studies prior to this investigation. The US was performed with a 14−5 MHz linear transducer on a Toshiba Xario 200 scanner (Nasushiobara, Tochigi, Japan). The optic nerve in ultrasound images appears as a hypoechoic tubular structure in the retrobulbar fat [7,31,32]. The axis of the nerve is assessed by following an ophthalmic artery located in the center of the nerve using color Doppler technique [33]. The ONSD was measured in each eye with an electronic caliper, using the axis perpendicular to the optic nerve, about 3-mm depth behind the globe [1,7,8,10–14,22,26,30,34,35] as shown in Fig. 1. There were 63 patients who had US of the optic nerve to evaluate optic nerve sheath diameter in our cohort.

2. Material and methods 2.1. Study population The study was approved by our hospital Ethics Committee. Informed consent was required from all patients whom had undergone US of ONSD. The investigation included all consecutive adult patients (age > 15 years) presenting to our trauma center for care of TBI who received head CT in the Emergency Department (ED) from July 2015 to October 2016. Patients who had past history of eye surgery, glaucoma or suspected of having optic nerve diseases were excluded. 2.2. Clinical assessment Demographic data including gender, age, blood pressure, temperature, heart rate, mechanism of injury and Glasgow Coma Scale (GCS) for evaluating severity of TBI were collected from medical records.

3. Statistical analysis Descriptive statistics for baseline demographic data were calculated. The continuous variables were summarized as mean or median, standard deviation (SD) depending on data distribution. The categorical variables were described as frequency and percentage. Categorical variables were calculated for sensitivity, specificity, negative predictive value (NPV), positive predictive value (PPV) and accuracy with 95 % confidence interval (95 %CI), and were compared using Pearson Chi-square or Fisher exact test. We chose cutoff values of greater than 4.8 mm for predicting increased ICP as per several past references [1,36]. Continuous variables were compared using Mann-Whitney U test or t-test. The correlation between two continuous variables was assessed with a Spearman correlation. Interobserver agreement was determined using Pearson correlation coefficient. Acceptable agreement between two readers for measurement of ONSD in CT is within a cutoff value of 0.6 mm. All analyses were performed using STATA version 13 (Stata Corp., College Station, Texas, USA). The p-value of less than 0.05 was considered statistically significant.

2.3. Image acquisition and imaging assessment 2.3.1. CT assessment A total of 271 consecutive patients underwent multidetector CT (MDCT) scan on a 128-slice scanner (Aquilion CX Toshiba Medical System Corporation, Tokyo, Japan) in our ED. The CT parameters were as follows: slice thickness of 1 mm, rotation time of 0.5-0.6 s, tube voltage of 120 kV, and tube current of 200−300 mA. All CT images were reconstructed in standard and high-spatial frequency algorithms with soft tissue setting (window level of 40 Hounsfield Units (HU) and a window width of 400 HU). The axial standard plane refers to the plane that derived from routine axial CT with slice thickness 2 mm. In addition to the standard plane, CT data were reformatted with an axial plane angled at -10° degrees to the orbitomeatal baseline for evaluating optic nerve [29], called optic-nerve axial plane. The optic nerve appeared almost straight and can be seen in its entire length from the optic canal to its entrance at the globe on this plane. Measurements of ONSD were measured by using electronic caliper in both axial standard plane and optic-nerve axial plane (ON axial plane) in the cut that the appearance optic nerves were optimally visualized. The retrobulbar area was zoomed 4 times to allow optic nerve sheath diameter (ONSD) to be measured in the axis perpendicular to the optic nerve (transverse plane) at the point 3 mm behind the globe of each eye [28,30] (shown in Fig. 1). All ONSDs were measured in each eye in both axial and ON axial planes. All measurement parameters were made using same window, contrast and brightness on Picture Archiving and Communication Systems (PACS; Synapse, version 3.2.0, FUJIFILM Medical Systems United States’ Synapse® PACS system, Stamford, Connecticut, United States) workstations. These measurements were made independently by two readers (PJ; 2 years of experience in emergency radiology and PT; 2nd-year neuroimaging fellow) who were unaware of patients’ clinical data except for a history of TBI. Discrepancies between two readers were rectified by the 3rd radiologist with 10 years of experience in emergency radiology (RK).

4. Results 4.1. Patient demographics (Table 1) There were 271 patients (127 males and 144 females) with a mean age of 65.15 years (range 16–96 years). The median of GCS was 15 (interquartile range; IQR = 10–15). One-hundred-and eighty-nine of 271 patients (69.74 %) had mild head injury, 57 (21.03 %) had moderate head injury and 25 patients (9.23 %) had severe head injury. The most common mechanism of injury was fall from standing (207 patients; 76.38 %). 4.2. CT findings CT findings are presented in Table 1. Intracranial hemorrhage (ICH) was the most common finding, found in 36 patients (13.28 %). The 2

European Journal of Radiology 125 (2020) 108875

P. Jenjitranant, et al.

Fig. 1. Measurement of ONSD by two modalities at approximately 3-mm depth behind the globe of a 90-year-old patient who presented with mild head injury but no intracranial hemorrhage, midline shift, brain herniation or other signs of increased intracranial pressure (A–C). The ONSDs measured by US (D–E), normal axial plane of CT (F) and optic-nerve axial plane of CT (G) are lower than the cutoff points; < 3.15 mm in US and < 4.8 mm in CT.

3

European Journal of Radiology 125 (2020) 108875

P. Jenjitranant, et al.

plane CT and US. The average ONSD was 4.70 ± 0.59 mm, 4.78 ± 0.59 mm and 3.16 ± 0.50 mm in the axial plane, ON axial plane and US, respectively. Significant difference was found between CT and US measurements with a p-value less than 0.05. The median variation of ONSD measured by CT and US was 1.43 mm (95 %CI = −0.07, 2.93) (Fig. 2). Table 4 compares ONSD between patients with and without various CT findings. The ONSD was significantly increased in the presence of diffuse sulcal effacement, effacement of basal cistern, brain herniation and intracranial hemorrhage. However, there was no significant difference in ONSD of patients with and without hydrocephalus or midline shift. Association between signs of increased ICP and ONSD in CT and US is shown in Table 5. The ONSD cutoff point for each sign in CT ranges from 4.8 to 5.0 mm. The ONSD cutoff point in CT at 4.8 mm for detection of any primary signs of increased intracranial pressure in CT had 60.5 % sensitivity, 61.2 % specificity, 20.4 % PPV, 90.4 % NPV and 61.1 % accuracy. The ONSD cutoff point in US at 3.15 mm for detection of any primary signs of increased intracranial pressure in CT had 97.4 % sensitivity, 13.8 % specificity, 15.7 % PPV, 97 % NPV and 25.6 % accuracy (Fig. 3).

Table 1 Patient characteristics and imaging findings. Characteristics and CT findings

Total (N=271)

Characteristics Age, years (range) Gender (n, %) Male Female Systolic blood pressure (mmHg) (mean ± SD) Diastolic blood pressure (mmHg) (mean ± SD) Temperature (°C) Heart rate (beat/min) (mean ± SD) Glasgow Coma Scale (GCS) (range) Head injury (n, %) Mild Moderate Severe Mechanisms (n, %) Fall Motor Vehicle Accident (MVA) Body assault CT findings Diffuse sulcal effacement Effacement of basal cistern Hydrocephalus Midline shift Imaging of brain herniation Hemorrhage Intraventricular hemorrhage (IVH) Intraparenchymal hemorrhage (IPH) Subdural hematoma (SDH) Subarachnoid hemorrhage (SAH) Epidural hematoma (EDH) Multi-compartmental hemorrhage Bone fracture

65.15 (16–96) 127(46.86%) 144(53.14%) 151.09 ± 31.83 79.69 ± 15.10 36.6 ± 2.13 83.26 ± 16.74 15 (10-15) 189 (69.74%) 57 (21.03%) 25 (9.23%) 207 (76.38%) 47 (17.35%) 17 (6.27%) 13 (4.81%) 8 (2.95%) 6 (2.21%) 5 (1.85%) 10 (3.69%) 36 (13.28%) 3 (9.09%) 12 (33.33%) 27 (79.41%) 18 (52.94%) 5 (14.71%) 1 (2.78%) 25 (9.43%)

5. Discussion There is a strong relationship between ONSD and increased ICP because optic nerve is located within subarachnoid space and connects with meningeal dura mater [37,38]. Therefore, increase in ICP can directly affect ONSD with an increasing pressure resulting in a greater ONSD [16–19]. Our study confirms this correlation between ONSD and primary CT signs of increased ICP found on CT, which is in line with that described by Legrand et al. [39]. We found that all primary CT findings of increased ICP were correlated with greater ONSD with most being significantly correlated except hydrocephalus and midline shift. Despite midline shift and hydrocephalus being previously described as important and specific CT signs of increased ICP [6,8,14,22,31,36], these two signs may take time to develop. In addition, there was a small number of patients with these two signs (5–6 patients each; 1.85–2.21 %) in our cohort therefore the correlation did not reach statistical significance. In recent years, US, CT and MRI have been proposed as an indirect, noninvasive and alternative means to diagnose increased ICP [1,5,7–15,25–28]. Our investigation compares ONSD measured by US and two CT planes in the same patients. We found no difference of ONSD measurement between axial CT plane and ON axial plane, suggesting that there is no need to perform a dedicated CT reformation of the optic nerve for its measurements. These can shorten time for CT postprocessing. Despite few reports [30] showing a good correlation of ONSD measured by CT and US, our investigations found a contrary. There was a significant difference of ONSD between CT and US with a median variation of 1.4 mm. We could not find a good explanation for this variation even after re-reviewing all US images along with their measurements as they were appropriately collected using standard protocol. Operator dependency of US might play a role for this discrepancy despite adequate training. The mean ONSD measured by CT in our

Table 2 Measurement of optic nerve sheath diameter (ONSD). ONSD (mm)

Total Right Male Female Left Male Female

Measurement CT axial plane

CT optic-nerve axial plane

US

(N = 271) 4.70 ± 0.59 4.69 ± 0.61 4.88 ± 0.61 4.52 ± 0.55 4.71 ± 0.65 4.90 ± 0.71 4.53 ± 0.55

(N = 271) 4.78 ± 0.59 4.75 ± 0.62 4.97 ± 0.64 4.56 ± 0.55 4.80 ± 0.64 4.98 ± 0.68 4.64 ± 0.55

(N = 63) 3.16 ± 0.50 3.15 ± 0.56 3.21 ± 0.56 3.10 ± 0.56 3.18 ± 0.59 3.23 ± 0.70 3.14 ± 0.49

most frequent location of ICH was subdural space (79.41 %). One of ICH patients (2.78 %) had multicompartmental hemorrhage. The second most frequent finding was skull fracture, found in 25 patients (9.43 %). The ONSD measured at CT in two planes and US were shown in Table 2. There was no significant difference of ONSD measured by two readers with an average difference of -0.135 mm (95 % level of agreement = -0.632 – 0.354). Table 3 compares ONSD measured on an axial-plane CT, ON axial Table 3 Comparison of ONSD measured by CT and US. ONSD measurement (mm) CT axial plane Total Right Left

4.70 ± 0.59 4.69 ± 0.61 4.71 ± 0.65

CT optic-nerve axial plane

p-value

US

p-value

4.78 ± 0.59 4.75 ± 0.62 4.80 ± 0.64

0.1128 0.2241 0.0839

3.16 ± 0.50 3.15 ± 0.56 3.18 ± 0.59

< 0.01* < 0.01* < 0.01*

* Statistically significant difference (p-value < 0.05). 4

European Journal of Radiology 125 (2020) 108875

P. Jenjitranant, et al.

Fig. 2. A: Comparison of ONSD measurement by CT and US. B: Median variation of ONSD measurement by CT and US after adding the value of median variation (1.4 mm), which results in ONSD measurements by US getting closer to those measured on CT.

Blaivas M et al. reported cutoff values of ONSD measured by US for diagnosis of elevated ICP at greater than 5 mm with high sensitivity, specificity, PPV and NPV [22]. Our study found cutoff values of ONSD measured by CT at 4.8 mm with low sensitivity and specificity (60.5 % and 61.2 %, respectively) but with high NPV (90.4 %). Given the high NPV, a cutoff value of < 4.8 mm may be used to exclude increased ICP. This information, in addition to clinical picture, may be worthwhile in ruling out increased ICP in a patient with unremarkable neurological examination. We believe that additional research should try to establish the normal versus abnormal ONSD value at CT in a more diverse group of patients, particularly in those without other signs of increased ICP because the normal ONSD could serve as another noninvasive marker of absence of increased ICP. This information may help expedite the care of emergency patients such as reduction of observation time or early discharge. Our investigation had several limitations. This was a retrospective study with limited sample size. The measurement of ONSD by US was performed by one operator, which may result in an information bias. Further inter-observer study for ONSD US is required. There was a small number of CT-positive patients therefore few CT findings were not shown to be correlated with ONSD. Lastly, we did not collect detailed information of severity of each CT signs of increased ICP.

Table 4 Association between ONSD measurement by CT (axial & ON-axial plane) and imaging findings in CT. Imaging abnormalities

Diffuse sulcal effacement - CT axial plane - CT optic-nerve axial plane Effacement of basal cistern - CT axial plane - CT optic-nerve axial plane Hydrocephalus - CT axial plane - CT optic-nerve axial plane Midline shift - CT axial plane - CT optic-nerve axial plane Brain herniation - CT axial plane - CT optic-nerve axial plane Intracranial hemorrhage - CT axial plane - CT optic- nerve axial plane

ONSD (mm) Absent

Present

p-value

4.82 ± 0.54 4.91 ± 0.52

5.47 ± 1.21 5.66 ± 1.25

0.0001* 0.0001*

4.67 ± 0.54 4.75 ± 0.91

5.57 ± 1.29 5.73 ± 1.28

0.0000* 0.0000*

4.69 ± 0.58 4.77 ± 0.59

5.14 ± 0.74 5.14 ± 0.74

0.0609 0.1293

4.69 ± 0.59 4.77 ± 0.59

5.10 ± 0.39 5.27 ± 0.33

0.1225 0.0609

4.68 ± 0.55 4.76 ± 0.55

5.28 ± 1.11 5.41 ± 1.15

0.0013* 0.0006*

4.66 ± 0.55 4.74 ± 0.55

4.94 ± 0.76 5.01 ± 0.79

0.0064* 0.0123*

* Statistically significant difference (p-value < 0.05).

study was 4.70 ± 0.59 mm which is consistent with previous studies [13,40]. However, mean ONSD measured by US was 3.16 ± 0.50 mm, which is lower than previous investigations. We believe that, in our scenario, CT is more accurate for measuring ONSD than US since the measurements were performed by two readers with validated and precise techniques. US is an operator dependent imaging and images used for measurement is 2D, which might not display the exact shadow of ONSD when angled differently [41]. Additionally, ONSD measurement may be limited by patient factors or operator experience. [42]. Some studies also reported inter-observer disagreement for measuring ONSD by US [41,43].

6. Conclusion In summary, there was a significant association between ONSD and primary CT signs of increased ICP with high NPV. No significant difference of ONSD measured on axial-plane CT and ON axial plane, therefore, measurement with routine axial CT was considered adequate for evaluating increased ICP. A size of ONSD of less than 4.8 mm measured by CT was a useful indicator for excluding increased ICP. We cannot recommend ONSD US as a sole measure for increased ICP given a significant difference between US and CT-measured ONSD at 1.4 mm.

Table 5 : Performance between ONSD and positive imaging findings. Positive brain injury CT - Hemorrhage - Diffuse sulcal effacement - Effacement of basal cistern - Hydrocephalus - Midline shift - Brain herniation - Any US Any

N (%)

Cutoff point (mm)

ROC (95% CI)

Sensitivity

Specificity

PPV

NPV

Accuracy

22 (8.12%) 7 (2.58%) 6 (2.21%) 3 (1.11%) 4 (1.48%) 7 (2.58%) 23 (8.49%)

4.8 5.0 4.9 5.0 4.9 4.9 4.8

61.2 63.9 70.6 61.6 72.9 68.1 60.7

(52.5-69.9) (49.5-78.2) (54.3-86.9) (39.5-83.7) (53.1-92.7) (52.9-83.4) (51.5-69.9)

61.1% 53.8% 75% 50% 80% 70% 60.5%

61.3% 73.9% 66.2% 73.2% 65.8% 66.3% 61.2%

19.5% 9.5% 6.3% 4.1% 4.2% 7.37% 20.4%

91.1% 96.9% 98.9% 98.5% 99.4% 98.3% 90.4%

64.2% 73.0% 66.4% 72.7% 66.1% 66.4% 61.1%

37 (13.65%)

3.15

69.5 (50.4-88.6)

97.4%

13.8%

15.7%

97%

25.6%

5

European Journal of Radiology 125 (2020) 108875

P. Jenjitranant, et al.

Fig. 3. Positive correlation between increased ICP and ONSD. Axial (A–B) and right-sagittal (C) CT images of a 90-year-old patient who presented with mild head injury reveals signs of increased ICP such as left frontal hemorrhagic cerebral contusion and right-sided extra-axial hemorrhages in the posterior cranial fossa with diffuse sulcal effacement. The ONSD measured by both US (D–E) and CT (F–G) are higher than the cutoff points; > 3.15 mm in US and > 4.8 mm in CT.

Funding

Disclosures

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Pinporn Jenjitranant: no any relevant financial relationships with any commercial interest. Padcha Tunlayadechanont: no any relevant financial relationships with any commercial interest. Thidathit Prachanukool: no any relevant financial relationships with any commercial interest.

Grant information None 6

European Journal of Radiology 125 (2020) 108875

P. Jenjitranant, et al.

Rathachai Kaewlai: no any relevant financial relationships with any commercial interest.

Anaesth. Intensive Care 39 (1) (2011) 95–100. [22] M. Blaivas, D. Theodoro, P.R. Sierzenski, Elevated intracranial pressure detected by bedside emergency ultrasonography of the optic nerve sheath, Acad. Emerg. Med. 10 (April (4)) (2003) 376–381. [23] The joint section on neurotrauma and critical care. Use of Mannitol, J. Neurotrauma. 17 (6_7) (2000) 521–525. [24] S.M. Iencean, A.V. Ciurea, Intracranial hypertension: classification and patterns of evolution, J. Med. Life 1 (2) (2008) 101–107. [25] T. Geeraerts, S. Merceron, D. Benhamou, B. Vigue, J. Duranteau, Noninvasive assessment of intracranial pressure using ocular sonography in neurocritical care patients, Intensive Care Med. 34 (November (11)) (2008) 2062–2067. [26] C.G. Shirodkar, K. Munta, S.M. Rao, M.U. Mahesh, Correlation of measurement of optic nerve sheath diameter using ultrasound with magnetic resonance imaging, Indian J. Crit. Care Med. 19 (8) (2015) 466–470. [27] G.W. Hassen, O. Nazeer, F. Manizate, N. Patel, H. Kalantari, The role of bedside ultrasound in pretherapeutic and posttherapeutic lumbar puncture in patient with idiopathic intracranial hypertension, Am. J. Emerg. Med. 32 (October (10)) (2014) 1298 e3-4. [28] H. Kalantari, R. Jaiswal, I. Bruck, H. Matari, F. Ghobadi, J. Weedon, et al., Correlation of optic nerve sheath diameter measurements by computed tomography and magnetic resonance imaging, Am. J. Emerg. Med. 31 (November (11)) (2013) 1595–1597. [29] R. Unsold, J. DeGroot, T.H. Newton, Images of the optic nerve: anatomic-CT correlation, Am. J. Roentgenol. 135 (4) (1980) 767–773. [30] G.W. Hassen, I. Bruck, J. Donahue, B. Mason, B. Sweeney, W. Saab, et al., Accuracy of optic nerve sheath diameter measurement by emergency physicians using bedside ultrasound, J. Emerg. Med. 48 (4) (2015) 450–457. [31] A.A. Malayeri, S. Bavarian, M. Mehdizadeh, Sonographic evaluation of optic nerve diameter in children with raised intracranial pressure, J. Ultrasound Med. 24 (2) (2005) 143–147. [32] J. Ballantyne, A.S. Hollman, R. Hamilton, M.S. Bradnam, R. Carachi, D.G. Young, et al., Transorbital optic nerve sheath ultrasonography in normal children, Clin. Radiol. 54 (11) (1999) 740–742. [33] T.H. Williamson, A. Harris, Color Doppler ultrasound imaging of theeye and orbit, Surv. Ophthalmol. 40 (4) (1996) 255–267. [34] K. Helmke, M. Burdelski, H.C. Hansen, Detection and monitoring of intracranial pressure dysregulation in liver failure by ultrasound, Transplantation 70 (July(2)) (2000) 392–395. [35] T. Soldatos, D. Karakitsos, K. Chatzimichail, M. Papathanasiou, A. Gouliamos, A. Karabinis, Optic nerve sonography in the diagnostic evaluation of adult brain injury, Crit. Care 12 (3) (2008) R67-R. [36] V. Rajajee, M. Vanaman, J.J. Fletcher, T.L. Jacobs, Optic nerve ultrasound for the detection of raised intracranial pressure, Neurocrit. Care 15 (December (3)) (2011) 506–515. [37] C. Robba, G. Santori, M. Czosnyka, F. Corradi, N. Bragazzi, L. Padayachy, et al., Optic nerve sheath diameter measured sonographically as non-invasive estimator of intracranial pressure: a systematic review and meta-analysis, Intensive Care Med. 44 (8) (2018) 1284–1294. [38] D.M. Nusbaum, S.M. Wu, B.J. Frankfort, Elevated intracranial pressure causes optic nerve and retinal ganglion cell degeneration in mice, Exp. Eye Res. 136 (July) (2015) 38–44. [39] A. Legrand, P. Jeanjean, F. Delanghe, J. Peltier, B. Lecat, H. Dupont, Estimation of optic nerve sheath diameter on an initial brain computed tomography scan can contribute prognostic information in traumatic brain injury patients, Crit. Care 17 (2) (2013) R61. [40] L. Romagnuolo, V. Tayal, C. Tomaszewski, T. Saunders, H.J. Norton, Optic nerve sheath diameter does not change with patient position, Am. J. Emerg. Med. 23 (September (5)) (2005) 686–688. [41] H. Hossein-Nejad, M. Bahreini, F. Rasooli, Bias in the measurement of optic nerve sheath diameter, Am. J. Emerg. Med. 36 (2) (2018) 323–324. [42] C.M. Woster, M.D. Zwank, J.R. Pasquarella, S.S. Wewerka, J.P. Anderson, J.T. Greupner, et al., Placement of a cervical collar increases the optic nerve sheath diameter in healthy adults, Am. J. Emerg. Med. 36 (3) (2018) 430–434. [43] S. Oberfoell, D. Murphy, A. French, S. Trent, D. Richards, I inter-rater reliability of sonographic optic nerve sheath diameter measurements by emergency medicine physicians, J. Ultrasound Med. 36 (August (8)) (2017) 1579–1584.

References [1] T. Geeraerts, Y. Launey, L. Martin, J. Pottecher, B. Vigué, J. Duranteau, et al., Ultrasonography of the optic nerve sheath may be useful for detecting raised intracranial pressure after severe brain injury, Intensive Care Med. 33 (10) (2007) 1704–1711. [2] P.B. Donald, J.D. Miller, D.W. John, P.G. Richard, F.Y. Harold, S. Romas, The outcome from severe head injury with early diagnosis and intensive management, J. Neurosurg. 47 (4) (1977) 491–502. [3] F.M. Lawrence, W.S. Randall, M.S. Harvey, The outcome with aggressive treatment in severe head injuries, J. Neurosurg. 50 (1) (1979) 20–25. [4] J. Han, S. Yang, C. Zhang, M. Zhao, A. Li, Impact of intracranial pressure monitoring on prognosis of patients with severe traumatic brain injury: a PRISMA systematic review and meta-analysis, Medicine (Baltimore) 95 (7) (2016) e2827. [5] H.H. Kimberly, S. Shah, K. Marill, V. Noble, Correlation of optic nerve sheath diameter with direct measurement of intracranial pressure, Acad. Emerg. Med. 15 (2) (2008) 201–204. [6] S.M. Fernando, A. Tran, W. Cheng, B. Rochwerg, M. Taljaard, K. Kyeremanteng, et al., Diagnosis of elevated intracranial pressure in critically ill adults: systematic review and meta-analysis, Br. Med. J. 366 (2019) l4225. [7] K. Helmke, H.C. Hansen, Fundamentals of transorbital sonographic evaluation of optic nerve sheath expansion under intracranial hypertension, Pediatr. Radiol. 26 (10) (1996) 701–705. [8] W.D. Newman, A.S. Hollman, G.N. Dutton, R. Carachi, Measurement of optic nerve sheath diameter by ultrasound: a means of detecting acute raised intracranial pressure in hydrocephalus, Br. J. Ophthalmol. 86 (10) (2002) 1109. [9] G. Cammarata, G. Ristagno, A. Cammarata, G. Mannanici, C. Denaro, A. Gullo, Ocular Ultrasound to detect Intracranial hypertension in trauma patients, J. Trauma 71 (3) (2011) 779–781. [10] J. Dubourg, E. Javouhey, T. Geeraerts, M. Messerer, B. Kassai, Ultrasonography of optic nerve sheath diameter for detection of raised intracranial pressure: a systematic review and meta-analysis, Intensive Care Med. 37 (7) (2011) 1059–1068. [11] J. Bäuerle, M. Nedelmann, B-mode sonography of the optic nerve in neurological disorders with altered intracranial pressure, Perspect. Med. 1 (1) (2012) 404–407. [12] R. Moretti, B. Pizzi, F. Cassini, N. Vivaldi, Reliability of optic nerve ultrasound for the evaluation of patients with spontaneous intracranial hemorrhage, Neurocrit. Care 11 (3) (2009) 406–410. [13] A.S. Girisgin, E. Kalkan, S. Kocak, B. Cander, M. Gul, M. Semiz, The role of optic nerve ultrasonography in the diagnosis of elevated intracranial pressure, Emerg. Med. J. 24 (4) (2007) 251–254. [14] V.S. Tayal, M. Neulander, H.J. Norton, T. Foster, T. Saunders, M. Blaivas, Emergency department sonographic measurement of optic nerve sheath diameter to detect findings of increased intracranial pressure in adult head injury patients, Ann. Emerg. Med. 49 (4) (2007) 508–514. [15] R. Major, S. Girling, A. Boyle, Ultrasound measurement of optic nerve sheath diameter in patients with a clinical suspicion of raised intracranial pressure, Emerg. Med. J. 28 (8) (2011) 679. [16] R. Moretti, B. Pizzi, Ultrasonography of the optic nerve in neurocritically ill patients, Acta Anaesthesiol. Scand. 55 (6) (2011) 644–652. [17] H.E. Killer, H.R. Laeng, J. Flammer, P. Groscurth, Architecture of arachnoid trabeculae, pillars, and septa in the subarachnoid space of the human optic nerve: anatomy and clinical considerations, Br. J. Ophthalmol. 87 (6) (2003) 777–781. [18] D. Liu, M. Kahn, Measurement and relationship of subarachnoid pressure of the optic nerve to intracranial pressures in fresh cadavers, Am. J. Ophthalmol. 116 (5) (1993) 548–556. [19] D. Liu, J. Michon, Measurement of the subarachnoid pressure of the optic nerve in human subjects, Am. J. Ophthalmol. 119 (1) (1995) 81–85. [20] G.J. du Toit, D. Hurter, M. Nel, How accurate is ultrasound of the optic nerve sheath diameter performed by inexperienced operators to exclude raised intracranial pressure? SA J. Radiol. 19 (1) (2015). [21] D.W. Potgieter, A. Kippin, F. Ngu, C. McKean, Can accurate ultrasonographic measurement of the optic nerve sheath diameter (a non-invasive measure of intracranial pressure) be taught to novice operators in a single training session?

7