Neurocrit Care

https://doi.org/10.1007/s12028-019-00762-z

ORIGINAL WORK

Ratio of Optic Nerve Sheath Diameter

to Eyeball Transverse Diameter by Ultrasound
Can Predict Intracranial Hypertension
in Traumatic Brain Injury Patients: A Prospective
Study
Jie Du1†, Yanjun Deng1†, Hua Li1, Shigang Qiao1,2, Mengnan Yu1, Qingya Xu1 and Chen Wang1,2*

© 2019 Springer Science+Business Media, LLC, part of Springer Nature and Neurocritical Care Society

Abstract 
Background:  Measuring optic nerve sheath diameter (ONSD), an indicator to predict intracranial hypertension, is
noninvasive and convenient, but the reliability of ONSD needs to be improved. Instead of using ONSD alone, this
study aimed to evaluate the reliability of the ratio of ONSD to eyeball transverse diameter (ONSD/ETD) in predicting
intracranial hypertension in traumatic brain injury (TBI) patients.
Methods:  We performed a prospective study on patients admitted to the Surgery Intensive Care Unit. The included
52 adults underwent craniotomy for TBI between March 2017 and September 2018. The ONSD and ETD of each
eyeball were measured by ultrasound and computed tomography (CT) scan within 24 h after a fiber optic probe was
placed into lateral ventricle. Intracranial pressure (ICP) > 20 mmHg was regarded as intracranial hypertension. The cor-
relations between invasive ICP and ultrasound-ONSD/ETD ratio, ultrasound-ONSD, CT-ONSD/ETD ratio, and CT-ONSD
were each analyzed separately.
Results:  Ultrasound measurement was successfully performed in 94% (n = 49) of cases, and ultrasound and CT meas-
urement were performed in 48% (n = 25) of cases. The correlation efficiencies between ultrasound-ONSD/ETD ratio,
ultrasound-ONSD, CT-ONSD/ETD ratio, and ICP were 0.613, 0.498, and 0.688, respectively (P < 0.05). The area under
the curve (AUC) values of the receiver operating characteristic (ROC) curve for the ultrasound-ONSD/ETD ratio and
CT-ONSD/ETD ratio were 0.920 (95% CI 0.877–0.964) and 0.896 (95% CI 0.856–0.931), respectively. The corresponding
threshold values were 0.25 (sensitivity of 90%, specificity of 82.3%) and 0.25 (sensitivity of 85.7%, specificity of 83.3%),
respectively.
Conclusion:  The ratio of ONSD to ETD tested by ultrasound may be a reliable indicator for predicting intracranial
hypertension in TBI patients.
Keywords:  Eyeball transverse diameter, Intracranial hypertension, Optic nerve ultrasound, Traumatic brain injury

*Correspondence: anesthesia_chen@163.com
†
Jie Du and Yanjun Deng contributed equally to this manuscript.
1
Department of Anesthesiology and Perioperative Medicine, The
Affiliated Suzhou Science and Technology Town Hospital of Nanjing
Medical University, Suzhou Science and Technology Town Hospital, No. 1
Lijiang Road, Gaoxin District, Suzhou 215153, Jiangsu Province, China
Full list of author information is available at the end of the article
Introduction
Traumatic brain injury (TBI) accounts for 17–23% of
all traumas, and its disability rate and mortality top all
other types [1]. High intracranial pressure (ICP), a seri-
ous pathophysiology of TBI, leads to poor prognosis [2].
ICP can be used for detecting intracranial change, guid-
ing treatment, and controlling mortality [3] of TBI. At
present, ICP monitoring methods, such as ICP monitor
and lumbar puncture manometry, are invasive. Intraven-
tricular manometry is the gold standard of ICP monitor-
ing, but its wide use is restricted by high cost and special
equipment [4]. In addition, conventionally used lumbar
puncture manometry is not suitable for patients with
brain hernia after acute craniocerebral trauma. Moreo-
ver, both methods are associated with a high risk of
bleeding or infection.
Ultrasound is an ICP monitoring method that is safe,
available, reliable, and noninvasive. A large number of
studies testified that ultrasound measured optic nerve
sheath diameter (ultrasound-ONSD) can predict intrac-
ranial hypertension [5–7]. However, the use of this
indicator is limited [8, 9]. First, the factors affecting the
ONSD are still unclear. Second, the normal range or
threshold of ONSD for diagnosing intracranial hyperten-
sion is uncertain, and the two ranges may overlap. Third,
the reliability of ONSD needs to be improved.
To improve the reliability of ONSD measurement, the
ONSD to eyeball transverse diameter (ETD) ratio was
introduced [10]. Previous studies have shown the possi-
bility for the ONSD/ETD ratio to indicate ICP [10–13],
and this ratio had no significant correlation with gen-
der, ethnicity, age, and body mass index (BMI) [14, 15].
A recent study confirmed the usefulness of this index in
diagnosing traumatic cerebral hemorrhage [16]. In those
studies, ultrasound or computed tomography (CT) was
generally used to measure ONSD, and magnetic reso-
nance imaging (MRI) or CT was used to measure ETD.
Results have shown that the values of ONSD or ETD
measured by ultrasound are in good agreement with
those by MRI or CT [17–20]. However, both MRI and CT
cannot be easily performed on TBI patients. This study
aimed to evaluate the accuracy of the ONSD/ETD ratio
measured by ultrasound.
Methods
Ethical Approval
This prospective study was approved by the institutional
review board of Suzhou Science and Technology Town
Hospital (IRB2019007). Informed consent was collected
from the family members of all patients.
Patients
Between March 2017 and September 2018, 105 patients
with TBI in the surgery intensive care unit (SICU) were
enrolled. All patients underwent craniotomy within 24 h
after admission. An ICP probe was placed in the lateral
ventricle. Exclusion criteria were as follows: (1) previ-
ous ocular and optic nerve diseases, (2) combined ocu-
lar and optic nerve injuries at admission, (3) lack of ICP
monitoring and/or insufficient sedation (Richmond Agi-
tation-Sedation Scale ≥ 1), (4) age less than 18  years, (5)
pretraumatic diseases in important organs (heart, lung,
kidney, etc.) or mental disorder, and (6) polytrauma and/
or traumatic shock. Fifty two individuals underwent both
ultrasound and CT measurements (Fig. 1). Patients were
managed according to current TBI guidelines [21].
Clinical Data Collection
General data at admission were recorded: gender, age,
height, weight, Glasgow coma score (GCS), heart rate,
blood pressure, and BMI. Postadmission condition was also
recorded using ONSDs, ETDs, ICPs, pupil’s abnormality,
mechanical ventilation, and sedation.
PRESSIO ICP Monitoring System (SOPHYSA, France)
was used to continuously measure ICP by invasive intra-
ventricular manometry. ICP > 20  mmHg indicated the
presence of intracranial hypertension [22]. The instru-
ment was operated by neurosurgeons with routine clini-
cal practice in the operating room [21]. The ICP values
were recorded by a clinical doctor (Li Hua). ONSD
and ETD values were measured by ultrasound and CT.
The ultrasound and CT operators were blinded to the
patient’s ICP values.
Ultrasound measurement was performed at the bed-
side by an experienced operator (Yu Mengnan). Here, a
6- to 13-MHz linear array ultrasonic probe from Edge
(Sonosite Corporation, USA), a portable color ultrasound
instrument, was used. ONSD and ETD were measured in
the SICU within 24 h after surgery. The patient was in a
supine position with the head in the middle and the eye-
lids closed. The probe was placed horizontally above the
transverse axis of the eyeball (Fig. 1a) and then slowly and
vertically moved to the eyeball from the patient’s fore-
head to the nose until the clearest and artifact-free opti-
mal plane was echoed on the frozen images. The optic
nerve image was a low-echo strip structure located in the
front and rear of the eyeball. The simultaneous appear-
ance of lens and optic nerve meant the ultrasound probe
was on the best plane. After removing the probe, the
optic nerve and the sheaths on its two sides were visible
with distinct margins. The maximum external diameter
of ONSD (ultrasound-ONSD) at 3  mm behind the ball
and the maximum diameter of ETD (parallel lens) on this
plane were measured (Fig. 1b). Both eyes were measured
 Fig. 1  Flow diagram
thrice, and the values were averaged as the final ONSD
and ETD.
CT measurement was performed within 1 h after ultra-
sound measurement. The 256-row Philips Brilliance iCT
(Philips, Netherlands) was used. The scanning condi-
tions were 120  kV, auto mA, 512 × 512, 5.0  mm thick,
and 1 mm reconstruction. During CT examination, con-
scious patients were advised to keep both their head and
eyeballs in natural position. Other operations were the
same as those in ultrasound examination. Simultane-
ous appearance of the lens and optic nerve directed the
best measurement plane (Fig. 1c). The maximum external
diameter of ONSD (CT-ONSD) and the maximum diam-
eter of ETD on this plane (parallel lens) were measured
(Fig.  1d). All CT images were measured with the same
window, contrast, and brightness and by the same person
(Xu Qingya) using iMed Pacs Dicom Viewer version 4.1
(DHCC Corporation, CHINA).
CT and ultrasound operators were not the same per-
son and did not know each other’s task. Each patient was
measured once.
Statistical Analysis
Categorical variables were reported as frequencies and
percentages, and continuous variables were reported as
the mean ± standard deviation values. Normality test of
data used the single-sample K-S test. Pearson correla-
tion analysis was used to measure the normal distribu-
tion data. The optimal threshold values of the ONSD/
ETD ratio and ONSD for predicting intracranial hyper-
tension were determined by the AUC of ROC curve,
and their sensitivity and specificity were calculated.
The consistency among ultrasound-ONSD/ETD ratio,
ultrasound-ONSD, and ICP results were examined by
nonparametric methods, and ROC curves were com-
pared using the nonparametric methods described by
DeLong [23].
All statistical tests were two-tailed, and P < 0.05 was
considered statistically significant. Calculations were per-
formed with IBM SPSS version 20.0 (IBM, USA).
Results
Characteristics of Study Subjects
No significant ocular and optic nerve injuries and com-
plications associated with implanted ICP probe were
observed in any patients.
Ultrasound measurement succeeded in 94% (n = 49)
of cases and failed in three patients due to unclear ultra-
sound images. Of 49 patients (33 males and 16 females;
38 cases with GCS 3–8 on admission; 25 cases with
severe TBI), 18 patients displayed subdural hematoma,
8 epidural hematoma, 16 subarachnoid hemorrhage, 5
brain contusion, and 2 intracerebral hemorrhage. The
general ultrasound and CT information of patients at
admission are shown in Table 1.
Ultrasound and CT measurements succeeded in
48% (n = 25) of cases and failed in 27 patients due
Table 1 General information on  admission of  patients intracranial hypertension was all consistent with that
with ultrasound and CT measurements of intraventricular manometer results (Kappa = 0.710,
Demographic data (n, %)/(mean ± SD) (n,  %)/(mean ± SD) P < 0.05; Kappa = 0.602, P < 0.05; Kappa = 0.745,
Ultrasound (n = 49) CT (n = 25) P < 0.05), and the diagnostic efficiency of ultrasound-
ONSD/ETD and CT-ONSD/ETD was in good agree-
Gender-male 33 (67%) 14 (56%)
ment (Kappa = 0.757, P < 0.001).
Diagnosis
Subdural hematoma 18 (37%) 8 (32%)
Discussion
Epidural hematoma 8 (16%) 7 (28%)
In the present study, ONSD and ETD measured with
Subarachnoid hemorrhage 16 (33%) 6 (24%)
ultrasound and CT were compared with those with intra-
Brain contusion 5 (10%) 3 (12%)
ventricular manometry, the gold standard of ICP moni-
Intracerebral hemorrhage 2 (4%) 1 (4%)
toring. Our results showed that the diagnostic accuracy
Age 50 ± 10 51 ± 13
of ultrasound-ONSD/ETD ratio and ONSD was 85.7%
BMI 24 ± 3 25 ± 3
and 79.6%, respectively. There was a significant differ-
SBP 152 ± 33 158 ± 43
ence in the area under the ROC curve between ONSD/
DBP 90 ± 17 94 ± 14
ETD and ONSD (P < 0.05). The Kappa tests of ONSD/
MAP 111 ± 20 115 ± 22
ETD ratio, ONSD, and ICP showed that the ONSD/ETD
HR 86 ± 19 77 ± 21
ratio had diagnostic consistency with the gold standard.
GCS-median (IQP) 8 (6) 6 (5)
Moreover, the ratio had a more advantage of consist-
RASS-median (IQP) − 1(0) − 1(0)
ency compared with ONSD (Kappa = 0.710, P < 0.05 vs.
BMI body mass index, CT computed tomography, DBP diastolic blood pressure, Kappa = 0.602, P < 0.05), suggesting that the ONSD/ETD
GCS Glasgow Coma Score, HR heart rate, MAP mean arterial pressure, RASS
Richmond Agitation-Sedation Scale, SBP systolic blood pressure, SD standard
ratio could not only accurately predict the ICP increase
deviation but also represent a more accurate and valuable metric
for clinical research than ONSD.
Our data reinforced the work of others who have
shown that the CT-ONSD/ETD ratio is a more accu-
rate index for increased ICP than ONSD alone [10].
to unclear ultrasound images (n =  3), unclear CT However, the threshold value of the ultrasound-ONSD/
images (n = 8) and no optimal CT measurement plane ETD ratio in predicting intracranial hypertension was
(n = 16). Of 25 patients assessed by CT (14 males and 0.25, which is lower than that in Vaiman’s study (0.29 by
11 females; 18 cases with GCS 3–8 at admission; 16 CT) [13]. The reasons are as follows. First, the position
cases with severe TBI), eight patients displayed sub- and diameter of the intraorbital optic nerve are differ-
dural hematoma, seven epidural hematoma, six suba- ent. In this study, we measured the ONSD of the optic
rachnoid hemorrhage, three brain contusion, and one nerve 3  mm posterior to the posterior eyeball. At this
intracerebral hemorrhage (Fig. 2). point, the nerve diameter changes most significantly
Table  2 presents P values and r/t values between [24], while Vaiman CT-scanned a 8- to 12-mm portion
variables. We did not identify a correlation between behind the eyeball. Second, the severity of the disease
ONSD and ONSD/ETD ratio with indexes, such as always changes over time. Our study failed to measure
age, BMI, GCS score, or gender. Table  3 presents the the ONSD and ETD at the early stage of brain injury
results of the measurements under ultrasound and CT. when emergency surgery must be provided, and ONSD
The ICP of all patients ranged from − 5 to 80 mmHg. might also be affected by subsequent treatments. Third,
The accuracy comparison of ultrasound-ONSD/ETD the methods of ICP monitoring are different. This study
ratio, ultrasound-ONSD, and CT-ONSD/ETD ratio is adopted intraventricular manometry, while other stud-
shown in Table  4. The AUC of ROC curve was 0.920 ies used lumbar puncture manometry. Further study is
(95% CI 0.877–0.964), 0.870 (95% CI 0.798–0.910), required to compare the efficiency of intraventricular
and 0.896 (95% CI 0.856–0.931)(Fig.  3a), and the cor- manometry and lumbar puncture manometry.
responding threshold values were 0.25 (sensitivity of Another finding of this study was that the diagnos-
90%, specificity of 82.3%), 5.53 mm (sensitivity of 80%, tic power of the ONSD/ETD ratio based on ultrasound
specificity of 79.3%) and 0.25 (sensitivity of 85.7%, and CT was consistent (Kappa = 0.757, P < 0.001). We
specificity of 83.3%), respectively (Fig. 3b). found that ultrasound was more sensitive than CT
The predictive effect of ultrasound-ONSD/ (90% vs. 85.7%), while CT was more specific (82.3% vs.
ETD, ultrasound-ONSD, and CT-ONSD/ETD on 83.3%). However, both methods were consistent with the
 Fig. 2  a Optic nerve ultrasound examination. b Gray-scale image of eyeball, the ONSD is a linear hypoechoic structure posterior to the eyeball.
Caliper ONSD identifies the measured point 3 mm posterior to the eyeball. c Axial CT scans showing a postoperation CT image with normal ICP. d
The ONSD at 4.5 mm of the same patient. The CT-ONSD/ETD ratio is 0.19

Table 2  Correlation between ONSD, ETD, ONSD/ETD, and general admission data. Pearson correlation test for correlation
analysis of measurement data, and independent t test for correlation analysis between counting data and measurement
data
Variable ONSD ETD ONSD/ETD
R/t P R/t P R/t P

Age − 0.163 0.518 − 0.030 0.907 − 0.132 0.602

Height 0.398 0.102 0.505* 0.033 0.087 0.731
Weight 0.315 0.204 0.503* 0.033 − 0.014 0.958
BMI 0.147 0.560 0.283 0.256 − 0.049 0.848
SBP 0.009 0.971 0.071 0.780 0.060 0.813
DBP 0.065 0.799 0.037 0.885 0.045 0.858
MAP 0.042 0.868 − 0.017 0.948 0.058 0.819
HR 0.450 0.061 − 0.052 0.839 0.502 0.056
GCS 0.173 0.492 0.122 0.629 0.085 0.738
RASS 0.037 0.884 0.350 0.154 − 0.253 0.311
Gender 0.254 0.803 − 0.325 0.750 0.556 0.586
Pupil change 0.508 0.623 0.624 0.541 0.134 0.895
Pupil light reaction 1.308 0.255 0.374 0.714 1.262 0.225
BMI body mass index, DBP diastolic blood pressure, ETD eyeball transverse diameter, GCS Glasgow Coma Score, HR heart rate, MAP mean arterial pressure, ONSD optic
nerve sheath diameter, RASS Richmond Agitation-Sedation Scale, SBP systolic blood pressure, SD standard deviation
*P <0.05
Table 3 Optic nerve sheath and  eyeball measurements ultrasound-ONSD/ETD ratio may be valuable for pre-
by  ultrasound and  CT and  the ONSD/ETD ratio in  TBI dicting intracranial hypertension in TBI patients; how-
patients ever, further study is required before the ONSD/ETD
Variables Mean ± SD Maximum Minimum ratio can be used to make clinical decisions.
Some limitations need to be addressed. First, in this
Ultrasound measurement (n = 49) single-center, small-sample study, it is not possible to
ONSDa/ETD Left 0.252 ± 0.034 0.370 0.150 entirely blind the sonographer to the clinical details of
Right 0.255 ± 0.035 0.352 0.149 the patient, which leads to uncertainty in the measure-
Overall 0.253 ± 0.030 0.321 0.157 ment results. The study’s clinical practicability must
ONSDa (mm) Left 5.6 ± 0.8 8.3 3.3 be confirmed by multicenter and large-sample studies.
Right 5.7 ± 0.8 7.6 3.5 Second, the maximum CT-ETD and CT-ONSD were
Overall 5.7 ± 0.7 7.2 3.5 measured while both are in the same plane; otherwise,
ETD (mm) Left 22.28 ± 1.60 26.43 15.90 the CT-measured data were not used in our study. Thus,
Right 22.42 ± 1.40 27.03 18.95 CT measurements were not possible in 16 patients.
Overall 22.36 ± 1.41 26.23 18.68 However, in Vaiman’s study [13], as the optic nerve can
CT measurement (n = 25) have a sinuous course in the horizontal and the vertical
ONSDa/ETD Left 0.213 ± 0.029 0.302 0.151 plane, realignment in the optic nerve plane is needed
Right 0.202 ± 0.029 0.275 0.138 in some cases with measurement in several axes. Thus,
Overall 0.207 ± 0.025 0.259 0.158 more time may be required to measure the ONSD,
ONSDa (mm) Left 4.8 ± 0.7 6.5 3.6 making the ratio of CT-ONSD/ETD not feasible. Eye-
Right 4.5 ± 0.7 6.7 3.0 ball positioning during the measurement may affect
Overall 4.7 ± 0.6 6.1 3.6 the ONSD and ETD, and we only CT-measured ONSD
ETD (mm) Left 22.47 ± 1.17 24.60 20.30 at a point 3  mm posterior to the eyeball in this study.
Right 22.37 ± 1.23 25.40 19.80 Further studies are warranted to ascertain the optimal
Overall 22.43 ± 1.15 24.85 20.05 point. Third, this study does not show ICP changes dur-
CT computed tomography, ETD eyeball transverse diameter, ONSD optic nerve ing disease development, especially during emergency
sheath diameter, SD standard deviation, TBI traumatic brain injury surgery when we have no time to measure ONSD and
The overall value is the value for the left and right eyes combined ETD. Moreover, a major point for ONSD performance
a
  3 mm behind the eyeball
to predict increased ICP relies on the fact that cere-
brospinal fluid should be able to freely move from the
gold standard (Kappa = 0.710, P < 0.05; Kappa = 0.745, intracranial compartment to retrobulbar compartment.
P < 0.05). The ONSD/ETD ratio based on ultrasound or In case of intraventricular hemorrhage, CSF circulation
CT has the same diagnostic value for the ONSD/ETD can be altered, rending ONSD performance to predict
ratio. Given its high feasibility, our study finds that the raised ICP weaker.

Table 4  Accuracy comparison of the ultrasound-ONSD/ETD ratio and ultrasound-ONSD, and the CT-ONSD/ETD ratio
Accuracy indicators Ultrasound-ONSD/ETD ratio Ultrasound-ONSD (mm) CT-ONSD/ETD ratio

Threshold 0.25 5.53 0.25

Sensitivity 90% 80% 85.7%
Specificity 82.3% 79.3% 83.3%
Positive predictive value 78.3% 72.7% 66.7%
Negative predictive value 92.3% 85.2% 93.8%
Positive likelihood ratio 5.22 3.87 5.14
Negative likelihood ratio 12.1% 25.2% 17.1%
Accuracy rate 85.7% 79.6% 84%
Accuracy rate (95%CI) 0.920 0.870 0.896
(0.877–0.964)a (0.798–0.910) (0.856–0.931)
ETD eyeball transverse diameter, CI confidence intervals, ONSD optic nerve sheath diameter
a
  Compared with ONSD under ultrasound, P < 0.05
 Fig. 3  Receiver operating characteristic (ROC) curve of ONSD and ONSD divided by eyeball transverse diameter (ETD) for predicting increased ICP
(> 20 mmHg) under ultrasound in a. ROC curve of ONSD/ETD ratio for predicting increased ICP (> 20 mmHg) under CT in b
Conclusion
Ultrasound-ONSD/ETD may be a reliable indicator for
predicting intracranial hypertension in TBI patients.
Abbreviations
ONSD: Optic nerve sheath diameter; ICP: Intracranial pressure; ETD: Eyeball
transverse diameter; SICU: Surgery Intensive Care Unit; CT: Computed tomog-
raphy; AUC​: Area under curve; ROC: Receiver operating characteristic; GCS:
Glasgow Coma Score; BMI: Body mass index.
Author details
1
 Department of Anesthesiology and Perioperative Medicine, The Affiliated
Suzhou Science and Technology Town Hospital of Nanjing Medical University,
Suzhou Science and Technology Town Hospital, No. 1 Lijiang Road, Gaoxin
District, Suzhou 215153, Jiangsu Province, China. 2 Institute of Clinical Medi-
cine Research, The Affiliated Suzhou Science and Technology Town Hospital
of Nanjing Medical University, Suzhou Science and Technology Town Hospital,
No. 1 Lijiang Road, Gaoxin District, Suzhou 215153, Jiangsu Province, China.
Author’s Contributions
JD, YD, and CW conceived and designed the study. HL, MY, and QX performed
the experiments and analyzed the data. JD, YD wrote the paper. YD, SQ, and
CW reviewed and edited the manuscript. All authors discussed the results and
approved the manuscript.
Source of Support
There was no funding associated with this study.
Conflicts of interest
The authors declared that they have no conflicts of interest to this work.
Ethical Approval/Informed Consent
This study was conducted according to our institution’s guidelines for ethical
research. Institutional review board approval was obtained for this study
(IRB2019007).
 
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in pub-
lished maps and institutional affiliations.
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