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Noninvasive assessment of the intracranial pressure in non-traumatic intracranial hemorrhage
Journal of Clinical Neuroscience xxx (2016) xxx–xxx
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Clinical commentary
Noninvasive assessment of the intracranial pressure in non-traumatic intracranial hemorrhage Michael Vaiman a,⇑, Tal Sigal b, Itzhak Kimiagar c, Inessa Bekerman b a
Department of Otolaryngology – Head and Neck Surgery, Assaf Harofe Medical Center, Affiliated to Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv 6997801, Israel Department of Radiology, Assaf Harofe Medical Center, Affiliated to Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel c Department of Neurology, Assaf Harofe Medical Center, Affiliated to Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel b
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Article history: Received 16 March 2016 Accepted 25 June 2016 Available online xxxx Keywords: Adults Computed tomography (CT) scan Hemorrhagic stroke Intracranial pressure Non-traumatic intracerebral hemorrhage (ICH) Optic nerve sheath diameter
a b s t r a c t The article describes the modified technique of measuring the diameters of the optic nerve sheath (ONSD) for assessment of the intracranial pressure (ICP) in patients with intracerebral or subarachnoid hemorrhage (SAH). The CT scans of 443 patients were analyzed retrospectively. The ONSDs were measured at 3 mm behind the globe and at the point where the ophthalmic artery crosses the optic nerve. The ONSD/eyeball transverse diameter (ETD) ratio was calculated. The correlation analysis was performed with the Glasgow Coma Scale score, Hemispheric Stroke Scale score, Glasgow Outcome Score, and invasive ICP readings. ONSD was enlarged in 95% of patients with intracerebral hemorrhage or SAH. Pathological ONSDs were 6.6 ± 0.8 mm (cut-off value >5.5 mm; p < 0.05). ONSD/ETD ratio was 0.29 ± 0.05 against normative 0.19 ± 0.02 (p < 0.01) with no correlation with initial Glasgow Coma Scale score or Hemispheric Stroke Scale score. There was an inverse correlation between ONSD/ETD ratio and Glasgow Outcome Score (r = 0.7) and direct correlation with invasive ICP readings. This study provides further evidence that in patients with intracranial hemorrhage and SAH, the presence of ONSD greater than a threshold of 5.5 mm is significantly predictive of invasively measured elevated ICP. The prediction of raised ICP can be further refined by measuring ONSD at the point where the optic nerve and the ophthalmic artery cross, and by determining the ratio between the ONSD and ETD. Ó 2016 Elsevier Ltd. All rights reserved.
1. Introduction It is well documented that the hemorrhagic stroke or vascular abnormalities that resulted in intracerebral hemorrhage (ICH, parenchymal hemorrhage) or subarachnoid hemorrhage (SAH) almost inevitably lead to the elevated intracranial pressure (ICP) [1–4]. ICH and SAH may be caused by the spontaneous rupture of blood vessels damaged by chronic hypertension or amyloid angiopathy (primary) or by vascular malformations and aneurysms (secondary) [5]. While these two conditions have different clinical pictures and courses, different outcomes, and different treatment strategies, the elevated ICP is a common finding for them and decreasing of it is a part of their treatment because elevated ICP adds its share to an acute neurologic deficit. The quantitative diagnosis of elevated ICP can be obtained by various invasive detection methods but monitoring ICP changes in a clinical setting is difficult and several qualitative non-invasive ⇑ Corresponding author at: 33 Shapiro Street, Bat Yam 59561, Israel. Tel.: +972 3 553 6139; fax: +972 3 553 6137. E-mail address: [email protected] (M. Vaiman).
methods were also introduced into practice. Of them, CT scanning is used for more than 30 years and the measurement of the optic nerve sheath diameter (ONSD) is used for about 20 years. The ONSD method is based on the finding that the presence of the enlarged optic nerve sheath indicates the elevated ICP [6,7]. While we have no intention to reconfirm again the usefulness of the ONSD method in the current study, we paid attention to lacking of an established protocol of the procedure and to some disagreement between researches. In the emerging literature, various authors measured ONSD at different distances from the eye globe. Most of them measured it at 3 mm behind the globe [8–10], but some others measured it at 4 mm [11], 2 to 5 mm [12], 10 mm behind the globe [13], or did not mention the distance at all [14]. A normal/abnormal cut-off value of ONSD was independently set by different researches from 4.8 mm to P7.3 mm [6,9,15,16]. We demonstrated in our previous publications that the frequently used cut-off value of >5 mm can mislead a practitioner if the standard deviation of the data is taken into account and proposed the cut-off value of >5.5 mm that helps to avoid false positive results [13,17].
http://dx.doi.org/10.1016/j.jocn.2016.06.008 0967-5868/Ó 2016 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Vaiman M et al. Noninvasive assessment of the intracranial pressure in non-traumatic intracranial hemorrhage. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2016.06.008
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M. Vaiman et al. / Journal of Clinical Neuroscience xxx (2016) xxx–xxx
To increase accuracy of the ONSD method, it was suggested to use the ONSD to the eyeball transverse diameter (ETD) ratio as a possible index [13]. A strong correlation exists between the ETD and the ONSD and the ONSD/ETD ratio (index) can be calculated. This index provides accurate data for assessment of ICP changes and it equals 0.19 with standard deviation of only 0.02 if measured for the middle third of the optic nerve intraorbital path in healthy individuals [13,18,19]. The usefulness of this index was recently demonstrated for the cases of the traumatic head injury with hemorrhage [20]. The purpose of the current research was to modify the technique of measuring ONSDs for the ICP assessment in cases with non-traumatic ICH or SAH to make it an accurate diagnostic tool. Our aims were to establish the most accurate point to measure the ONSD in the intraorbital path of the optic nerve and to increase precision of the quantitative data. 2. Materials and methods 2.1. Study design and setting In a retrospective study, we collected and analyzed the CT scans of 443 adult patients (18+) that were admitted to the Department of Radiology from January 2011 to November 2015. The study protocol conformed to the ethical guidelines of the 1975 Declaration of Helsinki (amended 2013) as reflected a priori after approval by the Helsinki committee of our Medical Center. We examined the patients who were admitted to the Emergency Department, were referred for CT scans that included the head and neck region, and had non-traumatic ICH, SAH, or combined type of hemorrhage associated with a hemorrhagic stroke or vascular abnormalities. The subsequent investigation of these patients was performed after they were hospitalized to the intensive care unit or to the neurological department. The Hemispheric Stroke Scale (0 = good to 100 = bad) was used to assess patients with ICH [21]. The Glasgow Coma Scale based World Federation of Neurosurgical Societies Surgeons Grading System for Subarachnoid Hemorrhage (WFNS) scale was used to assess patients with SAH. Inclusion and exclusion criteria were as follows: The patients should not have open or closed head injury. All the selected patients should have confirmed diagnosis or ICH or SAH, at least two available CT scans, the Glasgow Coma Scale score, and the Glasgow Outcome Score. We excluded from the study patients with abnormalities of the sphenoid bone and the orbit, in addition to patients with traumatic brain injury and hemorrhages associated with existing brain tumor. Patients with documented ophthalmological or neuro-ophthalmological disorders were also excluded. In the current study the ONSD was measured at 3 mm behind the globe and at the point where the ophthalmic artery crosses the optic nerve (the anatomical landmark, 10 mm from the globe on average). The ONSD readings at 3 mm and at 10 mm from the globe were compared for false positive and false negative results for increased ICP and specificity and sensitivity for each position were calculated. In addition to the direct ONSD readings we measured the eyeball transverse diameter (ETD) and calculated the ONSD/ETD index (ratio). We used the ONSD/ETD index with cutoff value of >0.22 indicating the elevated ICP. 2.2. Data sources and measurements We analyzed data on the following variables: 1. ETD (retina to retina); 2. ONSD at 3 mm behind the globe 3. ONSD at the point where the optic nerve crosses the ophthalmic artery; 4. ONSD/ETD ratio; 5. The Hemispheric Stroke Scale score or the
WFNS scale score; 6. The Glasgow Coma Scale score; 7. The Glasgow Outcome Score; 8. sex; and 9. age of the participants. Analyzed CT scans were obtained by the 256-slice CT scanner (Brilliance iCT, Philips Healthcare), single slice section 0.6 mm. Initial assessments of the CT scans were performed by the radiologists on duty to detect the presence/absence of ICH or SAH or other types of intracranial hemorrhage at the time of admission. These radiologists detected the focal and/or diffuse hyperdense (acute SAH, ICH, and intraventricular hemorrhage) and hypodense (brain swelling) areas and the CT scan patterns specific for blood in the interhemispheric fissures [22]. Our initial aim was to confirm their diagnostic conclusions. When the diagnosis of ICH or SAH was confirmed, the left and right ETD and the ONSD were measured by the computer program at the same scan. The transverse (horizontal) diameter of the eyeball was used because the ONSD is usually measured in the transverse plain. Window parameters were: spine window, middle third; WW 60, WL 360, (sometimes abbreviated as C:60,0. W:360,0 spine), accuracy 1 pixel. All measurements were made using the same window, contrast and brightness. The error margin was expressed by means of the technical error of measurement (TEM) to calculate the intraevaluator variability and inter-evaluator variability between two evaluators. The same equipment and methodological procedures for measurements were adopted by both radiologists. 2.3. Analysis Measurements or data of nine selected variables were analyzed. A within-group repeated measures experimental statistical analysis was used to test the variables. To verify the normality of the data, normal probability plots and basic descriptive statistics (mean, standard deviation (SD), min, and max) were calculated for every variable. The data obtained from the left eyeball and the optic nerve and from the right eyeball and the nerve was compared. The correlation analysis was performed with sex and age groups (group I: 18–30; group II: 30–65; group III: 65+) and between the ONSD/ETD ratio and the Glasgow Coma Scale score upon admission and the Glasgow Outcome Score. The Student’s t-test and the non-parametric Mann–Whitney U-test were used to calculate ‘‘p” values, and the chi-squared test was applied to analyze correlations and to calculate ‘‘r” values. To calculate correlation coefficient between the ONSD/ETD ratio and the Glasgow Outcome Score we selected a subgroup of 68 patients to whom CT scan was performed four or five times and subsequent assessment of the condition was possible. Another subgroup consisted of 78 patients to whom invasive ICP measurement was applied. The cut-off value for the pathologically elevated ICP was 20 mm Hg. This subgroup was used to calculate any correlation between invasive and non-invasive measurements of the ICP levels. We used previously published normative data for ETD, ONSD, and ONSD/ETD index for comparison purposes [13,17–19]. The data were statistically evaluated by three-dimensional analysis of variance, SPSS, Standard version 17.0 (SPSS, Chicago, IL, 2007), and chi-squared test criterion using 95% confidence interval (r value). The level of significance for all analyses was set at p < 0.05. 3. Results We selected 443 patients that satisfied inclusion criteria from 1542 patients who were admitted to the Emergency Department and were further referred to ICU or Department of Neurology, Stroke Unit (M 194, F 118). The cohort had a mean age of 52 years (SD 17) and a median admission Glasgow Coma Scale score of 7 (interquartile range: 5–10). Of them, 200 patients had SAH, 188
Please cite this article in press as: Vaiman M et al. Noninvasive assessment of the intracranial pressure in non-traumatic intracranial hemorrhage. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2016.06.008
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M. Vaiman et al. / Journal of Clinical Neuroscience xxx (2016) xxx–xxx Table 1 Optic nerve sheath and eyeball diameter CT scan measurements (in mm) and the nerve sheath/eye index (ONSD/ETD ratio) Distance/position
Right eye
Left eye
Mean ± SD
Max
Min
Mean ± SD
Max
Min
Normative database ONSD-3 * ONSD-10**
4.94 ± 1.5 4.4 ± 0.8
7.5 5.6
3.5 3.3
5.17 ± 1.34 4.5 ± 0.6
7.9 5.9
3.8 3.3
Patients with ICH (n = 188) ONSD-3 ONSD-10
6.9 ± 1.7 6.6 ± 0.8
9.5 9.3
4.5 4.0
6.7 ± 1.6 6.6 ± 0.6
8.9 8.9
4.7 4.4
Patients with SAH (n = 200) ONSD-3 ONSD-10
7.3 ± 1.8 7.1 ± 1.1
9.7 9.4
4.5 4.2
7.2 ± 1.9 6.8 ± 0.8
9.3 9.3
4.3 4.4
All patients with pathology combined (n = 443) ONSD-3 7.1 ± 1.8 ONSD-10 6.9 ± 1.2 ETD 22.7 ± 1.5
9.7 9.4 25.2
4.5 4.0 20.0
6.9 ± 1.8 6.7 ± 1.1 22.9 ± 1.5
9.3 9.3 25.5
4.7 4.4 19.7
ONSD/ETD index** Normative ICH SAH Pathology patients
0.26 0.42 0.44 0.44
0.15 0.2 0.22 0.2
0.19 ± 0.02 0.29 ± 0.04 0.29 ± 0.05 0.29 ± 0.06
0.26 0.41 0.45 0.45
0.15 0.21 0.21 0.21
0.19 ± 0.01 0.29 ± 0.05 0.3 ± 0.05 0.29 ± 0.06
*
3 mm behind the globe 8–12 mm behind the globe at the point where the ophthalmic artery crosses the optic nerve. ETD = eyeball transverse diameter, ICH = intracerebral hemorrhage, ONSD = optic nerve sheath diameter, SAH = subarachnoid hemorrhage, SD = standard deviation. **
Table 2 p values and correlations between ETD and ONSD and analyzed variables. The Student’s t-test and the non-parametric Mann–Whitney U-test were used to calculate ‘‘p” values, and the chi-squared test was applied to analyze correlations and to calculate ‘‘r” values Variables
p
Normal ONSD vs. ONSD in pathology ONSD in pathology vs. age ONSD in pathology vs. sex Normal ONSD/ETD index vs. ONSD/ETD index in all pathology Normal ONSD/ETD index vs. ONSD/ETD index in ICH cases Normal ONSD/ETD index vs. ONSD/ETD index in SAH cases ICH ONSD vs. SAH ONSD ICH ONSD/ETD index vs. SAH ONSD/ETD index ONSD/ETD index in pathology and initial Glasgow Coma Scale score ONSD/ETD index in pathology and Glasgow Outcome Score (n = 68) ONSD/ETD index and the invasive ICP readings (n = 78) ONSD/ETD index and initial Hemispheric Stroke Scale score ONSD/ETD index and WFNS upon admission
0.02 0.37 0.48 <0.01 <0.01 <0.01 0.56 0.88
r
0.34 0.7 0.82 0.47 0.55
Significant values are in bold type. p < 0.05 was considered statistically significant. r = 0 represents no linear relationship, r = 1 represents perfect linear relationship. ETD = eyeball transverse diameter, ICH = intracerebral hemorrhage, ICP = intracranial pressure, ONSD = optic nerve sheath diameter, SAH = subarachnoid hemorrhage, SD = standard deviation, WFNS = World Federation of Neurosurgical Societies Surgeons Grading System for Subarachnoid Hemorrhage scale.
patients had ICH, and 55 patients presented combined forms including intraventricular hemorrhage. ICU mortality rate (excluding those who was pronounced dead upon admission to the Emergency Department or died at the Emergency Department before proper registration, initial CT scan, etc.) was 30% (n = 133). The analyzed charts indicate that all patients with suspected ICH, SAH, and other types of bleeding associated with the hemorrhagic stroke or vascular abnormalities underwent the initial noncontrast head CT scan that followed with a subsequent CT scan performed 12 hours later to evaluate the existing hemorrhage. In problematic patients and when recurrent bleeding was suspected more subsequent CT scans were prescribed. The radiologists were provided with relevant information, including time from onset of the pathological condition, relevant past history and current background information (use of anticoagulants, bleeding disorders, suspected malignancy, presence/absence of trauma, etc.). Average number of CT scans per patient was 2.8 (range 2–5) and altogether we examined 1240 CT scans. CT scan images presented acute SAH as linear hyperdense fluid collection within sulci and
fluid cisterns; hyperdense in appearance acute ICH was mostly found in frontal and temporal brain areas surrounded by edema in some patients; and intraventricular hemorrhage was seen as focal and diffuse hyperdensity within the ventricles settled mostly in the occipital horns. We measured 886 ETDs and 886 ONSDs (left and right). ETDs were measured once and ONSDs were measured for all subsequent CT scans. For the TEM calculation, two measurements were obtained by two evaluators from each variable (n =1772 measurements for ETD and ONSD by each of two evaluators). The difference between the first and second measurements were then determined and the relative TEM (technical error of measurement expressed in %) was calculated. For intra-evaluator TEM it was 3.2 for the ETD – acceptable, and 3.4 for the optic nerve sheath – acceptable. For inter-evaluator TEM it was 3.8 and 3.9 respectively (<5%, acceptable). ONSD was enlarged in 95% (420/443) of patients when CT scans indicated ICH or SAH. The mean ICP level obtained from invasive measurements was 27 mm Hg (n = 78). Table 1 presents the results
Please cite this article in press as: Vaiman M et al. Noninvasive assessment of the intracranial pressure in non-traumatic intracranial hemorrhage. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2016.06.008
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M. Vaiman et al. / Journal of Clinical Neuroscience xxx (2016) xxx–xxx
Table 3 Specificity and sensitivity of the optic nerve sheath diameter (ONSD) on CT scan and invasive investigations for the detection of the elevated intracranial pressure (ICP) (n = 78). The cut-off value >5.5 mm indicated pathologically enlarged ONSDs Variable
TP
FP
TN
FN
Specificity
Sensitivity
Investigations: ONSD-3 * ONSD-10** Invasive ICP readings
66 68 72
6 1 0
5 5 6
1 4 0
0.83 0.83 1
0.91 0.94 1
*
3 mm behind the globe 8–12 mm behind the globe at a point where the ophthalmic artery crosses the optic nerve. TP = true positive, FP = false positive, TN = true negative, FN = false negative. **
correlation between the non-invasively calculated the ONSD/ETD ratio and the invasively obtained ICP readings was very strong (r = 0.82). In repeated measurements, there was a correlation between decreasing of the ONSD/ETD ratio and increasing of the Glasgow Outcome Score (inverse correlation, r = 0.7). The ONSD readings taken at the anatomical landmark location indicate the elevated ICP more accurately if compared with the readings taken at 3 mm behind the globe (sensitivity 0.94 vs. 0.91, Table 3). 4. Discussion
Fig. 1. (A) Axial non-contrast CT scans showing an intracerebral hemorrhage in the right temporal lobe with right tentorial subdural hematoma caused by a ruptured aneurysm. (B) The measurement of the optic nerve sheath diameter (ONSD) of the same patient indicates the enlarged ONSD at 6.4 mm. The ONSD/eyeball transverse diameter (ETD) ratio is 0.29 against a normative of 0.19.
Fig. 2. Axial non-contrast CT scan. As the optic nerve can have a sinuous course in the horizontal and the vertical plane, realignment in the optic nerve plane is needed in some cases with measurement in several axes. When the ophthalmic artery is established as a landmark, the main measurement can be taken in the transverse plain at the point where the artery crosses the optic nerve. The current patient had an acute right subarachnoid hemorrhage and the right optic nerve sheath diameter is wider that than the left (7 mm vs. 6.6 mm, with the normal cut-off value at 5.5 mm).
ICH is characterized by bleeding directly into the brain tissue, and SAH characterized by bleeding into the cerebrospinal fluid surrounding the brain and spinal cord. As we see however from Table 1, 2 in general ICP elevation is approximately the same. From qualitative point of view, the wider ONSD corresponds with the actual pathology seen at the CT scans as can be observed in Figure 1A and B. We did not have enough evidence to report it in the Results section, but we observed a tendency of uneven widening of ONSD in many patients. For example, a patient with right SAH presented ONSD of 7 mm from the right eye and ONSD 6.6 mm from the left eye (Fig. 2). We plan additional research to clarify the matter, but most probably this disagreement in the readings arose because of uneven diameters of the left and the right optic canals [19]. The same Figure 2 illustrates another quality that should be further researched. The optic nerve might have almost a straight course from the papilla to the anterior lumen of the optic canal or might take a sinuous course via intraorbital space in the horizontal and the vertical planes. In some patients, when the ICP was increasing during the monitoring period and the ONSD was widening accordingly, we detected that the sinusoid became more prominent, i.e. the course was gradually moving from ‘‘I” line to ‘‘S” line. If such tendency is observed, an additional accuracy is needed to obtain correct readings. It is well known at list since 1980s [23] that since the optic nerve frequently has a sinuous course in the orbit, both CT scans in the horizontal and the vertical plane are to be analyzed. A section of the nerve in a single plane, can conduce a radiologist or a practitioner to overestimate or underestimate the ONSD. The analysis starts from the vertical plane (sagittal) images and then is followed by pixel to pixel analysis of the corresponding horizontal (coronal) images. 4.1. An attempt to increase precision of the quantitative data
of the measurements. At cut-off value >5.5 mm pathologically enlarged ONSDs were significantly wider than normal. ONSD/ETD ratio was 0.29 ± 0.06 against 0.19 ± 0.02 in healthy adults (p < 0.01). Table 2 presents p values and r values between analyzed variables. We did not find correlation between ONSD/ETD ratio with initial Glasgow Coma Scale score, initial Hemispheric Stroke Scale score, sex of the patients, and their age. The correlation with initial WFNS in patients with SAH was very slight (r = 0.55). The
Our approach was not to measure ONSD at a selected distance from the globe given in mm but to attach the point of ONSD measurement to some anatomical landmark. The ophthalmic artery crosses the optic nerve in the middle third of the nerve’s intraorbital path. Usually this cross is located 8–12 mm from the globe being insignificantly affected by the eyeball movements or deviations. While the specificity of readings obtained at 3 mm and
Please cite this article in press as: Vaiman M et al. Noninvasive assessment of the intracranial pressure in non-traumatic intracranial hemorrhage. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2016.06.008
M. Vaiman et al. / Journal of Clinical Neuroscience xxx (2016) xxx–xxx
10 mm behind the globe was the same (0.83, Table 3), ONSD at 10 mm from the globe have lower false positive results for increased ICP. The accuracy of the ONSD readings taken from this location was high enough to detect the elevated ICP in patients with pseudotumor cerebri [24]. As it was said in the Introduction, some disagreement exists in establishing the normal/pathological cut-off value for ONSD. Numerous reports on the subject indicate the standard deviation of the normative data that overlaps with the standard deviation of the pathological readings. Such situation can cause some uncertainty in evaluating the results. To present just one example, a report described patients with moderate brain injury having ONSD as 4.2 ± 1.2 mm while control healthy individuals had it as 3.6 ± 0.6 mm [25]. Definitely a practitioner might be perplexed of how to assess a reading of 4 mm. There are numerous similar examples in the papers on the topic. It is clearly observed in Table 1 that ONSDs taken farther from the globe have lesser standard deviation. We did not use cerebral perfusion pressure as an analyzed variable because the ONSD is not connected to it directly. In addition to changes in the cerebral blood flow edema around ICH also adds to ICP elevation. An increase in vasogenic edema may lead to secondary increase in ICP but we did not monitor this tendency most probably because the monitored patients (n = 68) were under active treatment. Among 68 monitored patients 23 died and we confirm that inverse correlation of ONSD/ETD index with the Glasgow Outcome Score predicted such outcome. 4.2. Limitation of the research All the CT scans were obtained by the 256-slice CT Philips scanner. It was recently reported that the ONSD measured by ultrasound was significantly higher than the ONSD measured by CT scan or MRI [26]. This study also found that comparability between ultrasound and CT scan or MRI seems to be less reliable than agreement between CT scan and MRI readings. It might be possible that results obtained by ultrasonography may differ from our data. 5. Conclusion This study provides further evidence that in patients with ICH and SAH the presence of ONSD greater than a threshold of 5.5 mm is significantly predictive of invasively measured elevated ICP. The current findings demonstrate that the prediction of raised ICP can be further refined by measuring ONSD at the point where the optic nerve and the ophthalmic artery cross, and by determining the ratio between the ONSD and ETD. Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. References [1] Moradiya Y, Ziai W. Intracranial pressure after aneurysmal subarachnoid hemorrhage: time to revisit. Crit Care Med 2015;43:253–4.
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[2] Qiu W, Jiang Q, Xiao G, et al. Changes in intracranial pressure gradients between the cerebral hemispheres in patients with intracerebral hematomas in one cerebral hemisphere. BMC Anesthesiol 2014;14:2014. http://dx.doi.org/ 10.1186/1471-2253-14-112. [3] Zoerle T, Lombardo A, Colombo A, et al. Intracranial pressure after subarachnoid hemorrhage. Crit Care Med 2015;43:168–76. [4] Steiner T, Juvela S, Unterberg A, et al. European Stroke Organization. European Stroke Organization guidelines for the management of intracranial aneurysms and subarachnoid haemorrhage. Cerebrovasc Dis 2013;35:93–112. [5] Qureshi AI, Tuhrim S, Broderick JP, et al. Spontaneous intracerebral hemorrhage. N Engl J Med 2001;344:1450–60. [6] Kimberly HH, Shah S, Marill K, et al. Correlation of optic nerve sheath diameter with direct measurement of intracranial pressure. Acad Emerg Med 2008;15:201–4. [7] Kimberly HH, Noble VE. Using MRI of the optic nerve sheath to detect elevated intracranial pressure. Crit Care 2008;12:181. http://dx.doi.org/10.1186/ cc7008. [8] Frumin E, Schlang J, Wiechmann W, et al. Prospective analysis of single operator sonographic optic nerve sheath diameter measurement for diagnosis of elevated intracranial pressure. West J Emerg Med 2014;15:217–20. [9] Legrand A, Jeanjean P, Delanghe F, et al. Estimation of optic nerve sheath diameter on an initial brain computed tomography scan can contribute prognostic information in traumatic brain injury patients. Crit Care 2013;17: R61. http://dx.doi.org/10.1186/cc12589. [10] Girisgin AS, Kalkan E, Kocak S, et al. The role of optic nerve ultrasonography in the diagnosis of elevated intracranial pressure. Emerg Med J 2007;24:251–4. [11] Passi N, Degnan AJ, Levy LM. MR imaging of papilledema and visual pathways: effects of increased intracranial pressure and pathophysiologic mechanisms. AJNR Am J Neuroradiol 2013;34:919–24. [12] Maude RJ, Barkhof F, Hassan MU, et al. Magnetic resonance imaging of the brain in adults with severe falciparum malaria. Malar J 2014;13:177. http://dx. doi.org/10.1186/1475-2875-13-177. [13] Vaiman M, Gottlieb P, Bekerman I. Quantitative relations between the eyeball, the optic nerve, and the optic canal important for intracranial pressure monitoring. Head Face Med 2014;10:32. http://dx.doi.org/10.1186/1746160X-10-32. [14] Ridha MA, Saindane AM, Bruce BB, et al. MRI findings of elevated intracranial pressure in cerebral venous thrombosis versus idiopathic intracranial hypertension with transverse sinus stenosis. Neuroophthalmology 2013;37:1–6. [15] Geeraerts T, Launey Y, Martin L, et al. Ultrasonography of the optic nerve sheath may be useful for detecting raised intracranial pressure after severe brain injury. Intensive Care Med 2007;33:1704–11. [16] Raboel PH, Bartek Jr J, Andresen M, et al. Intracranial pressure monitoring: invasive versus non-invasive methods – a review. Crit Care Res Pract 2012:950393. [17] Vaiman M, Abuita R, Bekerman I. Optic nerve sheath’ diameters in healthy adults measured by computer tomography. Int J Ophthalmol 2015;8:1240–4. http://dx.doi.org/10.3980/j.issn.2222-3959.2015.06.30. [18] Bekerman I, Gottlieb P, Vaiman M. Variations in eyeball diameters of the healthy adults. J Ophthalmol 2014:503645. http://dx.doi.org/10.1155/2014/ 503645. [19] Bekerman I, Kimiagar I, Sigal T, et al. Monitoring of intracranial pressure by CTdefined optic nerve sheath diameter. J Neuroimaging 2016;26:309–14. http:// dx.doi.org/10.1111/jon.12322. [20] Vaiman M, Sigal T, Kimiagar I, et al. Intracranial pressure assessment in traumatic head injury with hemorrhage via optic nerve sheath diameter. J Neurotrauma 2016 [Epub ahead of print]. [21] Adams RJ, Meador KJ, Sethi KD, et al. Graded neurologic scale for use in acute hemispheric stroke treatment protocols. Stroke 1987;18:665–9. [22] Osborn AG, editor. Diagnostic imaging. Brain. Salt Lake City: Amirsys Inc.; 2004. [23] Unsold R, DeGroot J, Newton TH. Images of the optic nerve: anatomic-CT correlation. AJR Am J Roentgenol 1980;135:767–73. [24] Bekerman I, Sigal T, Kimiagar I, et al. Diagnostic value of the optic nerve sheath diameter in pseudotumor cerebri. J Clin Neurosci 2016;30:106–9. http://dx. doi.org/10.1016/j.jocn.2016.01.018 [Epub ahead of print]. [25] Soldatos T, Karakitsos D, Chatzimichail K, et al. Optic nerve sonography in the diagnostic evaluation of adult brain injury. Crit Care 2008;12:R67. http://dx. doi.org/10.1186/cc6897. [26] Giger-Tobler C, Eisenack J, Holzmann D, et al. Measurement of optic nerve sheath diameter: differences between methods? A Pilot Study. Klin Monbl Augenheilkd 2015;232:467–70.
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Clinical commentary
Noninvasive assessment of the intracranial pressure in non-traumatic intracranial hemorrhage Michael Vaiman a,⇑, Tal Sigal b, Itzhak Kimiagar c, Inessa Bekerman b a
Department of Otolaryngology – Head and Neck Surgery, Assaf Harofe Medical Center, Affiliated to Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv 6997801, Israel Department of Radiology, Assaf Harofe Medical Center, Affiliated to Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel c Department of Neurology, Assaf Harofe Medical Center, Affiliated to Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel b
a r t i c l e
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Article history: Received 16 March 2016 Accepted 25 June 2016 Available online xxxx Keywords: Adults Computed tomography (CT) scan Hemorrhagic stroke Intracranial pressure Non-traumatic intracerebral hemorrhage (ICH) Optic nerve sheath diameter
a b s t r a c t The article describes the modified technique of measuring the diameters of the optic nerve sheath (ONSD) for assessment of the intracranial pressure (ICP) in patients with intracerebral or subarachnoid hemorrhage (SAH). The CT scans of 443 patients were analyzed retrospectively. The ONSDs were measured at 3 mm behind the globe and at the point where the ophthalmic artery crosses the optic nerve. The ONSD/eyeball transverse diameter (ETD) ratio was calculated. The correlation analysis was performed with the Glasgow Coma Scale score, Hemispheric Stroke Scale score, Glasgow Outcome Score, and invasive ICP readings. ONSD was enlarged in 95% of patients with intracerebral hemorrhage or SAH. Pathological ONSDs were 6.6 ± 0.8 mm (cut-off value >5.5 mm; p < 0.05). ONSD/ETD ratio was 0.29 ± 0.05 against normative 0.19 ± 0.02 (p < 0.01) with no correlation with initial Glasgow Coma Scale score or Hemispheric Stroke Scale score. There was an inverse correlation between ONSD/ETD ratio and Glasgow Outcome Score (r = 0.7) and direct correlation with invasive ICP readings. This study provides further evidence that in patients with intracranial hemorrhage and SAH, the presence of ONSD greater than a threshold of 5.5 mm is significantly predictive of invasively measured elevated ICP. The prediction of raised ICP can be further refined by measuring ONSD at the point where the optic nerve and the ophthalmic artery cross, and by determining the ratio between the ONSD and ETD. Ó 2016 Elsevier Ltd. All rights reserved.
1. Introduction It is well documented that the hemorrhagic stroke or vascular abnormalities that resulted in intracerebral hemorrhage (ICH, parenchymal hemorrhage) or subarachnoid hemorrhage (SAH) almost inevitably lead to the elevated intracranial pressure (ICP) [1–4]. ICH and SAH may be caused by the spontaneous rupture of blood vessels damaged by chronic hypertension or amyloid angiopathy (primary) or by vascular malformations and aneurysms (secondary) [5]. While these two conditions have different clinical pictures and courses, different outcomes, and different treatment strategies, the elevated ICP is a common finding for them and decreasing of it is a part of their treatment because elevated ICP adds its share to an acute neurologic deficit. The quantitative diagnosis of elevated ICP can be obtained by various invasive detection methods but monitoring ICP changes in a clinical setting is difficult and several qualitative non-invasive ⇑ Corresponding author at: 33 Shapiro Street, Bat Yam 59561, Israel. Tel.: +972 3 553 6139; fax: +972 3 553 6137. E-mail address: [email protected] (M. Vaiman).
methods were also introduced into practice. Of them, CT scanning is used for more than 30 years and the measurement of the optic nerve sheath diameter (ONSD) is used for about 20 years. The ONSD method is based on the finding that the presence of the enlarged optic nerve sheath indicates the elevated ICP [6,7]. While we have no intention to reconfirm again the usefulness of the ONSD method in the current study, we paid attention to lacking of an established protocol of the procedure and to some disagreement between researches. In the emerging literature, various authors measured ONSD at different distances from the eye globe. Most of them measured it at 3 mm behind the globe [8–10], but some others measured it at 4 mm [11], 2 to 5 mm [12], 10 mm behind the globe [13], or did not mention the distance at all [14]. A normal/abnormal cut-off value of ONSD was independently set by different researches from 4.8 mm to P7.3 mm [6,9,15,16]. We demonstrated in our previous publications that the frequently used cut-off value of >5 mm can mislead a practitioner if the standard deviation of the data is taken into account and proposed the cut-off value of >5.5 mm that helps to avoid false positive results [13,17].
http://dx.doi.org/10.1016/j.jocn.2016.06.008 0967-5868/Ó 2016 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Vaiman M et al. Noninvasive assessment of the intracranial pressure in non-traumatic intracranial hemorrhage. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2016.06.008
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M. Vaiman et al. / Journal of Clinical Neuroscience xxx (2016) xxx–xxx
To increase accuracy of the ONSD method, it was suggested to use the ONSD to the eyeball transverse diameter (ETD) ratio as a possible index [13]. A strong correlation exists between the ETD and the ONSD and the ONSD/ETD ratio (index) can be calculated. This index provides accurate data for assessment of ICP changes and it equals 0.19 with standard deviation of only 0.02 if measured for the middle third of the optic nerve intraorbital path in healthy individuals [13,18,19]. The usefulness of this index was recently demonstrated for the cases of the traumatic head injury with hemorrhage [20]. The purpose of the current research was to modify the technique of measuring ONSDs for the ICP assessment in cases with non-traumatic ICH or SAH to make it an accurate diagnostic tool. Our aims were to establish the most accurate point to measure the ONSD in the intraorbital path of the optic nerve and to increase precision of the quantitative data. 2. Materials and methods 2.1. Study design and setting In a retrospective study, we collected and analyzed the CT scans of 443 adult patients (18+) that were admitted to the Department of Radiology from January 2011 to November 2015. The study protocol conformed to the ethical guidelines of the 1975 Declaration of Helsinki (amended 2013) as reflected a priori after approval by the Helsinki committee of our Medical Center. We examined the patients who were admitted to the Emergency Department, were referred for CT scans that included the head and neck region, and had non-traumatic ICH, SAH, or combined type of hemorrhage associated with a hemorrhagic stroke or vascular abnormalities. The subsequent investigation of these patients was performed after they were hospitalized to the intensive care unit or to the neurological department. The Hemispheric Stroke Scale (0 = good to 100 = bad) was used to assess patients with ICH [21]. The Glasgow Coma Scale based World Federation of Neurosurgical Societies Surgeons Grading System for Subarachnoid Hemorrhage (WFNS) scale was used to assess patients with SAH. Inclusion and exclusion criteria were as follows: The patients should not have open or closed head injury. All the selected patients should have confirmed diagnosis or ICH or SAH, at least two available CT scans, the Glasgow Coma Scale score, and the Glasgow Outcome Score. We excluded from the study patients with abnormalities of the sphenoid bone and the orbit, in addition to patients with traumatic brain injury and hemorrhages associated with existing brain tumor. Patients with documented ophthalmological or neuro-ophthalmological disorders were also excluded. In the current study the ONSD was measured at 3 mm behind the globe and at the point where the ophthalmic artery crosses the optic nerve (the anatomical landmark, 10 mm from the globe on average). The ONSD readings at 3 mm and at 10 mm from the globe were compared for false positive and false negative results for increased ICP and specificity and sensitivity for each position were calculated. In addition to the direct ONSD readings we measured the eyeball transverse diameter (ETD) and calculated the ONSD/ETD index (ratio). We used the ONSD/ETD index with cutoff value of >0.22 indicating the elevated ICP. 2.2. Data sources and measurements We analyzed data on the following variables: 1. ETD (retina to retina); 2. ONSD at 3 mm behind the globe 3. ONSD at the point where the optic nerve crosses the ophthalmic artery; 4. ONSD/ETD ratio; 5. The Hemispheric Stroke Scale score or the
WFNS scale score; 6. The Glasgow Coma Scale score; 7. The Glasgow Outcome Score; 8. sex; and 9. age of the participants. Analyzed CT scans were obtained by the 256-slice CT scanner (Brilliance iCT, Philips Healthcare), single slice section 0.6 mm. Initial assessments of the CT scans were performed by the radiologists on duty to detect the presence/absence of ICH or SAH or other types of intracranial hemorrhage at the time of admission. These radiologists detected the focal and/or diffuse hyperdense (acute SAH, ICH, and intraventricular hemorrhage) and hypodense (brain swelling) areas and the CT scan patterns specific for blood in the interhemispheric fissures [22]. Our initial aim was to confirm their diagnostic conclusions. When the diagnosis of ICH or SAH was confirmed, the left and right ETD and the ONSD were measured by the computer program at the same scan. The transverse (horizontal) diameter of the eyeball was used because the ONSD is usually measured in the transverse plain. Window parameters were: spine window, middle third; WW 60, WL 360, (sometimes abbreviated as C:60,0. W:360,0 spine), accuracy 1 pixel. All measurements were made using the same window, contrast and brightness. The error margin was expressed by means of the technical error of measurement (TEM) to calculate the intraevaluator variability and inter-evaluator variability between two evaluators. The same equipment and methodological procedures for measurements were adopted by both radiologists. 2.3. Analysis Measurements or data of nine selected variables were analyzed. A within-group repeated measures experimental statistical analysis was used to test the variables. To verify the normality of the data, normal probability plots and basic descriptive statistics (mean, standard deviation (SD), min, and max) were calculated for every variable. The data obtained from the left eyeball and the optic nerve and from the right eyeball and the nerve was compared. The correlation analysis was performed with sex and age groups (group I: 18–30; group II: 30–65; group III: 65+) and between the ONSD/ETD ratio and the Glasgow Coma Scale score upon admission and the Glasgow Outcome Score. The Student’s t-test and the non-parametric Mann–Whitney U-test were used to calculate ‘‘p” values, and the chi-squared test was applied to analyze correlations and to calculate ‘‘r” values. To calculate correlation coefficient between the ONSD/ETD ratio and the Glasgow Outcome Score we selected a subgroup of 68 patients to whom CT scan was performed four or five times and subsequent assessment of the condition was possible. Another subgroup consisted of 78 patients to whom invasive ICP measurement was applied. The cut-off value for the pathologically elevated ICP was 20 mm Hg. This subgroup was used to calculate any correlation between invasive and non-invasive measurements of the ICP levels. We used previously published normative data for ETD, ONSD, and ONSD/ETD index for comparison purposes [13,17–19]. The data were statistically evaluated by three-dimensional analysis of variance, SPSS, Standard version 17.0 (SPSS, Chicago, IL, 2007), and chi-squared test criterion using 95% confidence interval (r value). The level of significance for all analyses was set at p < 0.05. 3. Results We selected 443 patients that satisfied inclusion criteria from 1542 patients who were admitted to the Emergency Department and were further referred to ICU or Department of Neurology, Stroke Unit (M 194, F 118). The cohort had a mean age of 52 years (SD 17) and a median admission Glasgow Coma Scale score of 7 (interquartile range: 5–10). Of them, 200 patients had SAH, 188
Please cite this article in press as: Vaiman M et al. Noninvasive assessment of the intracranial pressure in non-traumatic intracranial hemorrhage. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2016.06.008
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M. Vaiman et al. / Journal of Clinical Neuroscience xxx (2016) xxx–xxx Table 1 Optic nerve sheath and eyeball diameter CT scan measurements (in mm) and the nerve sheath/eye index (ONSD/ETD ratio) Distance/position
Right eye
Left eye
Mean ± SD
Max
Min
Mean ± SD
Max
Min
Normative database ONSD-3 * ONSD-10**
4.94 ± 1.5 4.4 ± 0.8
7.5 5.6
3.5 3.3
5.17 ± 1.34 4.5 ± 0.6
7.9 5.9
3.8 3.3
Patients with ICH (n = 188) ONSD-3 ONSD-10
6.9 ± 1.7 6.6 ± 0.8
9.5 9.3
4.5 4.0
6.7 ± 1.6 6.6 ± 0.6
8.9 8.9
4.7 4.4
Patients with SAH (n = 200) ONSD-3 ONSD-10
7.3 ± 1.8 7.1 ± 1.1
9.7 9.4
4.5 4.2
7.2 ± 1.9 6.8 ± 0.8
9.3 9.3
4.3 4.4
All patients with pathology combined (n = 443) ONSD-3 7.1 ± 1.8 ONSD-10 6.9 ± 1.2 ETD 22.7 ± 1.5
9.7 9.4 25.2
4.5 4.0 20.0
6.9 ± 1.8 6.7 ± 1.1 22.9 ± 1.5
9.3 9.3 25.5
4.7 4.4 19.7
ONSD/ETD index** Normative ICH SAH Pathology patients
0.26 0.42 0.44 0.44
0.15 0.2 0.22 0.2
0.19 ± 0.02 0.29 ± 0.04 0.29 ± 0.05 0.29 ± 0.06
0.26 0.41 0.45 0.45
0.15 0.21 0.21 0.21
0.19 ± 0.01 0.29 ± 0.05 0.3 ± 0.05 0.29 ± 0.06
*
3 mm behind the globe 8–12 mm behind the globe at the point where the ophthalmic artery crosses the optic nerve. ETD = eyeball transverse diameter, ICH = intracerebral hemorrhage, ONSD = optic nerve sheath diameter, SAH = subarachnoid hemorrhage, SD = standard deviation. **
Table 2 p values and correlations between ETD and ONSD and analyzed variables. The Student’s t-test and the non-parametric Mann–Whitney U-test were used to calculate ‘‘p” values, and the chi-squared test was applied to analyze correlations and to calculate ‘‘r” values Variables
p
Normal ONSD vs. ONSD in pathology ONSD in pathology vs. age ONSD in pathology vs. sex Normal ONSD/ETD index vs. ONSD/ETD index in all pathology Normal ONSD/ETD index vs. ONSD/ETD index in ICH cases Normal ONSD/ETD index vs. ONSD/ETD index in SAH cases ICH ONSD vs. SAH ONSD ICH ONSD/ETD index vs. SAH ONSD/ETD index ONSD/ETD index in pathology and initial Glasgow Coma Scale score ONSD/ETD index in pathology and Glasgow Outcome Score (n = 68) ONSD/ETD index and the invasive ICP readings (n = 78) ONSD/ETD index and initial Hemispheric Stroke Scale score ONSD/ETD index and WFNS upon admission
0.02 0.37 0.48 <0.01 <0.01 <0.01 0.56 0.88
r
0.34 0.7 0.82 0.47 0.55
Significant values are in bold type. p < 0.05 was considered statistically significant. r = 0 represents no linear relationship, r = 1 represents perfect linear relationship. ETD = eyeball transverse diameter, ICH = intracerebral hemorrhage, ICP = intracranial pressure, ONSD = optic nerve sheath diameter, SAH = subarachnoid hemorrhage, SD = standard deviation, WFNS = World Federation of Neurosurgical Societies Surgeons Grading System for Subarachnoid Hemorrhage scale.
patients had ICH, and 55 patients presented combined forms including intraventricular hemorrhage. ICU mortality rate (excluding those who was pronounced dead upon admission to the Emergency Department or died at the Emergency Department before proper registration, initial CT scan, etc.) was 30% (n = 133). The analyzed charts indicate that all patients with suspected ICH, SAH, and other types of bleeding associated with the hemorrhagic stroke or vascular abnormalities underwent the initial noncontrast head CT scan that followed with a subsequent CT scan performed 12 hours later to evaluate the existing hemorrhage. In problematic patients and when recurrent bleeding was suspected more subsequent CT scans were prescribed. The radiologists were provided with relevant information, including time from onset of the pathological condition, relevant past history and current background information (use of anticoagulants, bleeding disorders, suspected malignancy, presence/absence of trauma, etc.). Average number of CT scans per patient was 2.8 (range 2–5) and altogether we examined 1240 CT scans. CT scan images presented acute SAH as linear hyperdense fluid collection within sulci and
fluid cisterns; hyperdense in appearance acute ICH was mostly found in frontal and temporal brain areas surrounded by edema in some patients; and intraventricular hemorrhage was seen as focal and diffuse hyperdensity within the ventricles settled mostly in the occipital horns. We measured 886 ETDs and 886 ONSDs (left and right). ETDs were measured once and ONSDs were measured for all subsequent CT scans. For the TEM calculation, two measurements were obtained by two evaluators from each variable (n =1772 measurements for ETD and ONSD by each of two evaluators). The difference between the first and second measurements were then determined and the relative TEM (technical error of measurement expressed in %) was calculated. For intra-evaluator TEM it was 3.2 for the ETD – acceptable, and 3.4 for the optic nerve sheath – acceptable. For inter-evaluator TEM it was 3.8 and 3.9 respectively (<5%, acceptable). ONSD was enlarged in 95% (420/443) of patients when CT scans indicated ICH or SAH. The mean ICP level obtained from invasive measurements was 27 mm Hg (n = 78). Table 1 presents the results
Please cite this article in press as: Vaiman M et al. Noninvasive assessment of the intracranial pressure in non-traumatic intracranial hemorrhage. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2016.06.008
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M. Vaiman et al. / Journal of Clinical Neuroscience xxx (2016) xxx–xxx
Table 3 Specificity and sensitivity of the optic nerve sheath diameter (ONSD) on CT scan and invasive investigations for the detection of the elevated intracranial pressure (ICP) (n = 78). The cut-off value >5.5 mm indicated pathologically enlarged ONSDs Variable
TP
FP
TN
FN
Specificity
Sensitivity
Investigations: ONSD-3 * ONSD-10** Invasive ICP readings
66 68 72
6 1 0
5 5 6
1 4 0
0.83 0.83 1
0.91 0.94 1
*
3 mm behind the globe 8–12 mm behind the globe at a point where the ophthalmic artery crosses the optic nerve. TP = true positive, FP = false positive, TN = true negative, FN = false negative. **
correlation between the non-invasively calculated the ONSD/ETD ratio and the invasively obtained ICP readings was very strong (r = 0.82). In repeated measurements, there was a correlation between decreasing of the ONSD/ETD ratio and increasing of the Glasgow Outcome Score (inverse correlation, r = 0.7). The ONSD readings taken at the anatomical landmark location indicate the elevated ICP more accurately if compared with the readings taken at 3 mm behind the globe (sensitivity 0.94 vs. 0.91, Table 3). 4. Discussion
Fig. 1. (A) Axial non-contrast CT scans showing an intracerebral hemorrhage in the right temporal lobe with right tentorial subdural hematoma caused by a ruptured aneurysm. (B) The measurement of the optic nerve sheath diameter (ONSD) of the same patient indicates the enlarged ONSD at 6.4 mm. The ONSD/eyeball transverse diameter (ETD) ratio is 0.29 against a normative of 0.19.
Fig. 2. Axial non-contrast CT scan. As the optic nerve can have a sinuous course in the horizontal and the vertical plane, realignment in the optic nerve plane is needed in some cases with measurement in several axes. When the ophthalmic artery is established as a landmark, the main measurement can be taken in the transverse plain at the point where the artery crosses the optic nerve. The current patient had an acute right subarachnoid hemorrhage and the right optic nerve sheath diameter is wider that than the left (7 mm vs. 6.6 mm, with the normal cut-off value at 5.5 mm).
ICH is characterized by bleeding directly into the brain tissue, and SAH characterized by bleeding into the cerebrospinal fluid surrounding the brain and spinal cord. As we see however from Table 1, 2 in general ICP elevation is approximately the same. From qualitative point of view, the wider ONSD corresponds with the actual pathology seen at the CT scans as can be observed in Figure 1A and B. We did not have enough evidence to report it in the Results section, but we observed a tendency of uneven widening of ONSD in many patients. For example, a patient with right SAH presented ONSD of 7 mm from the right eye and ONSD 6.6 mm from the left eye (Fig. 2). We plan additional research to clarify the matter, but most probably this disagreement in the readings arose because of uneven diameters of the left and the right optic canals [19]. The same Figure 2 illustrates another quality that should be further researched. The optic nerve might have almost a straight course from the papilla to the anterior lumen of the optic canal or might take a sinuous course via intraorbital space in the horizontal and the vertical planes. In some patients, when the ICP was increasing during the monitoring period and the ONSD was widening accordingly, we detected that the sinusoid became more prominent, i.e. the course was gradually moving from ‘‘I” line to ‘‘S” line. If such tendency is observed, an additional accuracy is needed to obtain correct readings. It is well known at list since 1980s [23] that since the optic nerve frequently has a sinuous course in the orbit, both CT scans in the horizontal and the vertical plane are to be analyzed. A section of the nerve in a single plane, can conduce a radiologist or a practitioner to overestimate or underestimate the ONSD. The analysis starts from the vertical plane (sagittal) images and then is followed by pixel to pixel analysis of the corresponding horizontal (coronal) images. 4.1. An attempt to increase precision of the quantitative data
of the measurements. At cut-off value >5.5 mm pathologically enlarged ONSDs were significantly wider than normal. ONSD/ETD ratio was 0.29 ± 0.06 against 0.19 ± 0.02 in healthy adults (p < 0.01). Table 2 presents p values and r values between analyzed variables. We did not find correlation between ONSD/ETD ratio with initial Glasgow Coma Scale score, initial Hemispheric Stroke Scale score, sex of the patients, and their age. The correlation with initial WFNS in patients with SAH was very slight (r = 0.55). The
Our approach was not to measure ONSD at a selected distance from the globe given in mm but to attach the point of ONSD measurement to some anatomical landmark. The ophthalmic artery crosses the optic nerve in the middle third of the nerve’s intraorbital path. Usually this cross is located 8–12 mm from the globe being insignificantly affected by the eyeball movements or deviations. While the specificity of readings obtained at 3 mm and
Please cite this article in press as: Vaiman M et al. Noninvasive assessment of the intracranial pressure in non-traumatic intracranial hemorrhage. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2016.06.008
M. Vaiman et al. / Journal of Clinical Neuroscience xxx (2016) xxx–xxx
10 mm behind the globe was the same (0.83, Table 3), ONSD at 10 mm from the globe have lower false positive results for increased ICP. The accuracy of the ONSD readings taken from this location was high enough to detect the elevated ICP in patients with pseudotumor cerebri [24]. As it was said in the Introduction, some disagreement exists in establishing the normal/pathological cut-off value for ONSD. Numerous reports on the subject indicate the standard deviation of the normative data that overlaps with the standard deviation of the pathological readings. Such situation can cause some uncertainty in evaluating the results. To present just one example, a report described patients with moderate brain injury having ONSD as 4.2 ± 1.2 mm while control healthy individuals had it as 3.6 ± 0.6 mm [25]. Definitely a practitioner might be perplexed of how to assess a reading of 4 mm. There are numerous similar examples in the papers on the topic. It is clearly observed in Table 1 that ONSDs taken farther from the globe have lesser standard deviation. We did not use cerebral perfusion pressure as an analyzed variable because the ONSD is not connected to it directly. In addition to changes in the cerebral blood flow edema around ICH also adds to ICP elevation. An increase in vasogenic edema may lead to secondary increase in ICP but we did not monitor this tendency most probably because the monitored patients (n = 68) were under active treatment. Among 68 monitored patients 23 died and we confirm that inverse correlation of ONSD/ETD index with the Glasgow Outcome Score predicted such outcome. 4.2. Limitation of the research All the CT scans were obtained by the 256-slice CT Philips scanner. It was recently reported that the ONSD measured by ultrasound was significantly higher than the ONSD measured by CT scan or MRI [26]. This study also found that comparability between ultrasound and CT scan or MRI seems to be less reliable than agreement between CT scan and MRI readings. It might be possible that results obtained by ultrasonography may differ from our data. 5. Conclusion This study provides further evidence that in patients with ICH and SAH the presence of ONSD greater than a threshold of 5.5 mm is significantly predictive of invasively measured elevated ICP. The current findings demonstrate that the prediction of raised ICP can be further refined by measuring ONSD at the point where the optic nerve and the ophthalmic artery cross, and by determining the ratio between the ONSD and ETD. Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. References [1] Moradiya Y, Ziai W. Intracranial pressure after aneurysmal subarachnoid hemorrhage: time to revisit. Crit Care Med 2015;43:253–4.
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Please cite this article in press as: Vaiman M et al. Noninvasive assessment of the intracranial pressure in non-traumatic intracranial hemorrhage. J Clin Neurosci (2016), http://dx.doi.org/10.1016/j.jocn.2016.06.008