Transorbital Ultrasonographic Measurement of Optic Nerve Sheath Diameter for Intracranial Midline Shift in Patients with Head Trauma

Accepted Manuscript Transorbital ultra-sonographic measurement of optic nerve sheath diameter for intracranial midline shift in patients with head trauma Hizir Kazdal, Ayhan Kanat, Huseyin Findik, Ahmet Sen, Bulent Ozdemir, Osman Ersegun Batcik, Ozcan Yavasi, Mehmet Fatih Inecikli PII:

S1878-8750(15)01358-3

DOI:

10.1016/j.wneu.2015.10.015

Reference:

WNEU 3310

To appear in:

World Neurosurgery

Received Date: 9 September 2015 Revised Date:

30 September 2015

Accepted Date: 1 October 2015

Please cite this article as: Kazdal H, Kanat A, Findik H, Sen A, Ozdemir B, Batcik OE, Yavasi O, Inecikli MF, Transorbital ultra-sonographic measurement of optic nerve sheath diameter for intracranial midline shift in patients with head trauma, World Neurosurgery (2015), doi: 10.1016/j.wneu.2015.10.015. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ONSD and intracranial midline shift in intensive care unit

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Transorbital ultra-sonographic measurement of optic nerve sheath diameter for intracranial midline shift in patients with head trauma Hizir Kazdal (1), Ayhan Kanat (2), Huseyin Findik (3), Ahmet Sen (1), Bulent

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Ozdemir (2), Osman Ersegun Batcik (2), Ozcan Yavasi (4), Mehmet Fatih Inecikli (5)

1-Recep Tayyip Erdogan University Medical Faculty Department of Anesthesiology

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and Reanimation Rize-Turkey

2-Recep Tayyip Erdogan University, Medical Faculty, Department of Neurosurgery,

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Rize-Turkey

3-Recep Tayyip Erdogan University, Medical Faculty Department of Ophthalmology Rize-Turkey

Turkey.

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4-Recep Tayyip Erdogan University, Department of Emergency Medicine, Rize,

Rize, Turkey

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5- Recep Tayyip Erdogan University, Medical Faculty Department of Radiology,

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Correspond to:Ayhan Kanat, MD, Recep Tayyip Erdogan University, Medical Faculty, Department of Neurosurgery 53100 Merkez Rize Turkey, Mail to: [email protected] Phone: 90 5065855139

Fax 90 464 2140497

Keywords: transorbital ultra-sonography, optic nerve sheath diameter, intracranial midline shift, intensive care unit 1

ONSD and intracranial midline shift in intensive care unit

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Running title: optic nerve sheath diameter and intracranial midline shift Abstract

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Objective: Measurement of the optic nerve sheath diameter (ONSD) by using sonography is a straightforward, noninvasive technique to detect an increased

intracranial pressure, which can even be conducted at the bedside. However, the correlation

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between ONSD and intracranial midline shift has not been studied.

Methods: The authors performed a prospective, blinded observational study in

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intensive care unit (ICU). Patients were divided to groups. Of those, 19 patients had midline shift, whereas 26 had no intracranial pathology and shift, served as control individuals. Results: Forty-five patients were enrolled, ; Spearman rank correlation coefficient of difference of ONSD and midline shift was 0.761 (p < 0.0005) demonstrating a significant

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positive correlation between patient with midline shift and control group. Conclusions: Despite small numbers and selection bias, this study suggests that

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ONSD.

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bedside US may be useful in the diagnosis of midline intra cranial shift by measurement of

Keywords: transorbital ultra-sonography, optic nerve sheath diameter, intracranial

midline shift, intensive care unit

Running title: optic nerve sheath diameter and intracranial midline shift Introduction:

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ONSD and intracranial midline shift in intensive care unit

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Head trauma is a critical public health problem throughout the world. There may also be unrecognized changes in patient characteristics and management NIC (20). Patients with head trauma may have hematoma or develop cerebral edema, which can lead to increased

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intracranial pressure (ICP). Increased ICP leads to poor neurologic outcome in critical care unit. Prompt recognition and treatment are essential to prevent possible death. For that reason, periodic evaluation of neurointensive care (NIC) is important. A reliable non-invasive means

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to detect raised ICP is an important issue in the field of neuro-intensive care. While

papilledema is a long-recognized clinical sign of increased ICP, it can take many hours-to-

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weeks to develop (12). Standard techniques of invasive ICP monitoring, with either an intracerebral probe or an intraventricular catheter, may lead to hemorrhage as well as infection (24,28) In addition, it requires neurosurgical expertise (34), may be contraindications such as coagulopathy or thrombocytemia (27,38). In the absence of invasive

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monitoring, some signs such as edema, and the presence of midline shift in CT and MR may suggestive of increased ICP, (26), although it is not always easy task to take CT or MRI in the ICU setting (26), because these techniques need acquisition times, require patient

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transport which may be harmful for patients of ICU (8). While bedside ONSD on USG is known to be a sensitive screening test for elevated ICP in adult head injury, however, the

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diagnostic accuracy of ONSD ultrasound for intracranial midline shift remains unstudied. We sought to determine the feasibility of ONSD ultrasound as a screening tool for the evaluation of midline intracranial shift in ICU. To our knowledge, this is the first prospective study about this subject. Materials and methods: Study design: This was an observational study using a convenience sample of patients with head trauma presenting to an ICU between January 2014 to June 2015. This study was 3

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approved by the participating university's institutional research ethics committee, and performed in accordance with the ethical standards as laid down in the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards. Informed consent was

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obtained from all individual participants or relatives. Exclusion criteria included: eye injury or facial trauma, a history of elevated intraocular pressure, or eye disease that would reasonably preclude sonographic evaluation of the optic nerve. Patients were divided to groups. Of those,

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19 patients had midline shift due to head injury, whereas 26 had no intracranial pathology and shift, served as control individuals. Initially, brain-injured patients were evaluated clinically

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GCS (Glasgow Coma Scale). All patients underwent CT and synchronous ONSD measurements by optic nerve sonography. Computed tomography (CT) findings defined as indicative of ultra-sonographic measurement of optic nerve sheath diameter for patient group were the presence of mass effect with a midline shift. The patients of control group were also

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admitted with head injury. Cranial CT’s were obtained to exclude an intracranial pathology. In this group, there was no midline shift.

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Technique of optic nerve sonography

Bedside, blinded ONSD measurements were performed after patient admitted to the

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ICU. A 7.5 MHz transducer by bedside ultrasonography (Fazone CB, Fujifilm, USA) was used for measurement of ONSD. The examiner scanned both the eyes through closed eyelids in supine position. A thick layer of ultrasound gel was used to prevent pressure from being exerted on the eye. The probe was placed on the superior and lateral aspect of the orbit against the upper eyelid with the eye closed and angled slightly caudally and medially until the optic nerve was visualized as a linear hypoechoic structure with clearly defined margins posterior to the globe. Placement of the transducer was adjusted to bring the best angle for displaying the exit of the optic nerve from the globe. The position of the probe was adjusted to clearly 4

ONSD and intracranial midline shift in intensive care unit

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display the entry of the optic nerve into the globe. The widest visible retrobulbar ONSD was measured at a point 3 mm posterior to the posterior scleral surface of the globe using an inbuilt electronic caliper to the nearest millimetre; with an angle perpendicular to the eye ball.

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All measurements were made bilaterally. Because it was hypothesized that unilateral lesions most likely transmit pressure to parenchymal tissue on the same side, correlation of ONSD to midline herniation was performed separately for unilateral and then bilateral brain injuries.

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The optic disc was also evaluated by ophthalmoscopy by senior author (HF).

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Statistical methods:

Data were analyzed using the statistical package for the social sciences version 16 (SPSS Inc., Chicago, IL) and Stata/IC 10.0 (Stata Corporation, College Station, Texas) statistical software. Difference of ONSD between patient and control group were compared.

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Correlation test for midline shift and ONSD difference was performed. Variables were assessed with the one-way ANOVA test.

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Results:

Forty-five patients were underwent transorbital ultra-sonographic ONSD

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measurement. The average time to ocular ultrasound completion was 6 min. Overall there were 32 men and 13 women. The mean age was 56,5 years (standard deviation 13,64, range 29-93).Spearman rank correlation coefficient of difference of ONSD and midline shift was 0.761 (p < 0.0005) demonstrating a significant positive correlation between patient with midline shift and control group (Table 1). The one-way ANOVA test showed that ONSD was significantly different between group 1 (patient group) and Group 2 (Control group) (p=0.09<0.05). In 14 patients (73,7%), mean ONSD was larger in same side with intracranial lesion than opposite side. Table 2 shows fundus and shift crosstabulation of patient group. 5

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Papil edema was not seen in 4 patients despite presence of 6-10 mms midline shift. Table 3 shows the crosstabulation of ONSD and midline shift. Figure 1 show CT scan of patient with left hemisphere cerebral edema with 10,8 mm midline shift. Differences left and right ONSD

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of same patient are seen in Figure 2. ONSD of left eye is 4 mms larger than right side. Discussion

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Traumatic brain injury (TBI) is one of major contributor to death and disability

globally (14,22,31,40). The assessment of injury severity and prognosis are of primary

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concern in this kind of injury. (7). Intracranial pressure monitoring is a cornerstone of in patients with cerebral herniation and traumatic brain injury (22,23,30,32). However, currently , its usefulness has been questioned (2,21,35). The concept of focused ultrasonography has emerged seven decades ago (6). In 1996, Helmke and Hansen reported a study about the

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evaluation of the optic nerve sheath expansion under intracranial hypertension by transorbital sonography (13). Today, ONSD measurement using ocular ultrasonography is a usefull method for indirect assessment of ICP without specific contraindication. This technique was

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developed based on ocular anatomy. The optic nerve is as an outward form of the diencephalon during embryogenesis, and wrapped by a nerve sheath that is derived from three

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layers of meninges and protrudes toward the orbit (10,37). As a consequence of this communication, cerebrospinal fluid (CSF) can transfer freely between the intracranial and intraorbital subarachnoid space (11). Despite the recent developments in technology (16,17,25,36), midline intracranial shift is one of main complication associated with brain injury, leads to high morbidity and mortality. For that reason, the early prediction of midline intracranial shift in neuro-intensive care unit is an important problem. We found that midline shift leaded asymmetric enlargement of ONSD, which was significantly different between patient and control groups. In addition, fundus and shift crosstabulation of patient group 6

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showed that papil edema was not seen in four patients despite presence of 6-10 mms midline shift. For that reason, the measurement of ONSD in neuro-intensive care is important to identify subclinical cases with midline shift and increased ICP secondary brain injury and to

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allow prompt treatment The value of present study

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The intracranial space has a limited ability to compensate for extra volume caused by cerebral edema occurred by TBI. When the compensatory mechanisms for extra intracranial

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volume are exhausted, the ICP rises very quickly. The pressure–volume relationship is explained by the Monro–Kellie doctrine (9). The time factor is important, and even after a mild TBI, the ICP can be quickly increased and may lead to life-threatening brain herniation. An increase in the volume of one of the components contained within the intracranial space

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can only occur at the expense of the other intracranial structure. Unilateral lesions most likely transmit pressure to parenchymal tissue on the same side. There are many publications on the correlation between the increased ICP and ultrasonographic ONSD in Pubmed

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(8,13,18,26,34). However, estimation of increased ICP by neuroimaging has not been validated and cannot serve as the correlating parameter. Moreover, patients can have midline

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shift on neuroimaging without elevation of intracranial pressure. A correlation of the ONSD with an ipsilateral mass effect would be more interesting including its dynamics after initiation of treatment. There is not a report for assessing correlation between ONSD and midline shift in literature. This point makes our research novel.The sonographic assessment of ONSD requires only 6 minutes. At this time, it is clear that this measurement may eliminate a CT scan if a neurosurgical procedures is anticipated for patients with TBI in NCU. Although not yet established, the aforementioned ultrasound methods have been gradually integrated in neuromonitoring strategies due to the availability of ultrasound systems which allowed fast 7

ONSD and intracranial midline shift in intensive care unit

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and by the bed evaluation in the ICU (18). The advantages of ultrasound examination of the optic nerve head are that it is non-invasive, widely available, portable, rapidly performed, of relatively low cost, and it does not employ ionising radiation. To our knowledge, ours is the

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first observational study to explore the clinical utility of bedside ocular ultrasound measurement of ONSD in a population of patients with head trauma and midline shift.

Neuromonitoring is one of the most important aspects in a neurocritical care setting, therefore

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every contribution, especially in the noninvasive field is very important. Our study was

specifically designed to analyze the predictive value of ONSD for midline shift, and revealed

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that there was a correlation between midline shift at CT images and ONSD measurement. It is useful method for the detection of acute, and possibly hyperacute, midline shift. Indeed, papil edema is accepted as an indirect and late indicator of raised ICP (3). Increased ICP is a result of TBI. Out finding is important and may be lead to early neurosurgical intervention in

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patients with TBI, because Shimoda et al recently found that surgical management was associated with improvement of the outcome and mortality for patients with TBI (33). It is interesting that papil edema was not seen in four patients despite presence of 6-10 mms

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midline shift (see table 2). The subarachnoid space is in continuity with the perineural space, and there is evidence that cerebral spinal fluid exchange between the craniospinal

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subarachnoid space and It is reported that the optic nerve sheath extension had taken place regularly within minutes (11), so the development of papilledema can take hours to many days, however, early human studies have shown that an increase in ICP results in distension of the retrobulbar optic nerve sheath within seconds (11,13). In this study, ONSD was significantly different between patient and control group, (p<0.05), and mean ONSD of 14 patients (73,7%) was larger in same side with intracranial lesion than opposite side. The recognition of this fact is important. If indeed one is the first to report something and that

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something is of value (1,15). In addition, the present study gives the answer why we should use the measurement of ONSD in patients with TBI of NIC unit. To the best of our knowledge, and this is the first study of association of ONSD and midline shift. Of course,

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further prospective multicenter trials are needed to confirm our findings. Limitations of the study

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This study is a single center study with a relatively small sample size. The results

should be validated in larger trials. Increased ICP is one of important cause of midline shift in

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patients with traumatic brain injury. We did not obtain the ICP values of patients. This is one of limitation of our study. Another limitation of study is that severity of trauma and GCS scores were not evaluated. It is reported the GCS was introduced as a scoring system for patients with impaired consciousness after TBI (29), and is the current standard means of

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assessing a patient's level of consciousness (39). In this study, GCS were not analized since the GCS has repeatedly been criticized for its several failures to reflect verbal reaction in intubated patients of NIC unit (5). Despite these limitations, given the limited knowledge on

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the association of optic nerve sheath diameter and intracranial midline shift in NIC unit, the present study remains significant because it provides the first exploratory analysis of clinical

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significance of transorbital ultra-sonographic measurement of optic nerve sheath diameter. Conclusion:

We conducted a prospective study using USG to measure ONSD in patients with

cerebral midline herniation and compared the same with a control group. Our study demonstrated that ONSD by US should be used for the detection of midline intracranial shift at the bedside. This paper provides clinical strategies that will enhance neurosurgeon and clinicians’ assessment of midline intracranial shift. In some contexts, red flags mean that

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something important needs to be brought to immediate attention (19). The present study may provide a red flag and added dimension as a useful follow-up tool for patients in ICU, because it has no known adverse effects. Sonography is readily available, relatively cheap, and well

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tolerated by patients (3).Most importantly, the technique does not involve use of ionising radiation like CT (4). It is well known that obtaining CT or MRI in patients of ICU it is not always easy task (26). These techniques need acquisition times, require patient transport

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which may be harmful for patients in ICU (8).Interestingly, in this study, it was observed that fundus changes cannot be seen after the occurrence of midline shift, hence fundoscopy

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can be normal in the early stages in spite of important midline shift. This result means that the sonographic ONSD measurement, therefore, be beneficial as it provides the basis for monitoring patients with midline intracranial shift. Our finding would be of significant value in situations where there is clinical suspicion for midline shift and possible intracranial

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hypertension but invasive monitoring is unavailable or risky to perform. Evolving research, recent years have witnessed remarkable achievements in neuromonitoring and neuroanesthetic techniques, with a huge body of literature consisting of

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excellent studies in neuro-anaesthesiology, predicting outcome of patients following brain

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injury in intensive care unit are important issue. Our study, which is novel as as it provides the basis for monitoring patients with midline intracranial shift in critical care unit, therefore, be beneficial.Any contribution to our knowledge of the cause of the morbidity and mortality in intensive care unit will always welcome Conflict of interest: None Disclosure Statement: No competing financial interests exist References: 10

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Legends:

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Disclosure Statement: No competing financial interests exist

Table 1: Spearman rank correlation coefficient of difference of ONSD and midline

shift was 0.761 (p < 0.0005) demonstrating a significant positive correlation between patient with midline shift and control group. Table 2 shows fundus and shift crosstabulation of patient group. Papil edema was not seen in 4 patients despite presence of 6-10 mms midline shift. Table 3 shows the crosstabulation of ONSD and midline shift.

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Figure 1 show CT scan of patient with left hemisphere cerebral edema with 10,8 mm midline shift.

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Figure 2 shows the differences left and right ONSD of same patient.

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ACCEPTED MANUSCRIPT Correlations difference Correlation Coefficient

1,000 ,075

Sig. (2-tailed)

. ,761

N Shift

19

19

Correlation Coefficient

,075

1,000

Sig. (2-tailed)

,761

. 19

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N

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difference

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Spearman's rho

Shift

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Fundoscopy

Total

Total

<5

2

5

7

6-10

4

1

5

>11

0

7

7

6

13

19

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Shift

FE

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FN

Table: Fundoscopy and midline shift crosstabulation patient group, Papil edema was not seen in 4 patients despite presence of 6-10

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mms midline shift FN: Fundus normal, FE Fundus with edema

ACCEPTED MANUSCRIPT ONSD <5mm

Total

4

2

7

>10

6

1

5

12

7

5

7

19

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1

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Total

>10

<10mm

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shift

5-10mm

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ACCEPTED MANUSCRIPT Abbreviations: GCS: Glasgow coma scale

NIC: neurointensive care ICU: intensive care unit.

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ONSD: optic nerve sheath diameter

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ICP: intracranial pressure

M AN U

TBI: traumatic brain injury.

AC C

EP

TE D

US: ultrasound

ACCEPTED MANUSCRIPT This is an observational study in patient with head trauma and midline shift. This is the first study of association of diameter of optic nerve sheath and midline shift

AC C

EP

TE D

M AN U

SC

RI PT

Bedside US may be useful in the diagnosis of midline intra cranial shift.