Non-invasive assessment of intracranial pressure using ocular sonography in neurocritical care patients

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1 Intensive Care Med (2008) 34: DOI /s x ORIGINAL Thomas Geeraerts Sybille Merceron Dan Benhamou Bernard Vigué Jacques Duranteau Non-invasive assessment of intracranial pressure using ocular sonography in neurocritical care patients Received: 8 March 2008 Accepted: 2 May 2008 Published online: 29 May 2008 Ó Springer-Verlag 2008 The authors received no financial support for this work. T. Geeraerts ()) S. Merceron D. Benhamou B. Vigué J. Duranteau AP-HP, Département d Anesthésie- Réanimation Chirurgicale, Univ Paris-Sud, Centre Hospitalier Universitaire Bicêtre, Le Kremlin Bicêtre, France thgeeraerts@hotmail.com Tel.: Fax: Abstract Objective: To assess the relationship between optic nerve sheath diameter (ONSD) and intracranial pressure (ICP) in neurocritical care patients. Design: Prospective, observational study. Setting: Surgical critical care unit, level 1 trauma center. Patients: A total number of 37 adult patients requiring sedation and ICP monitoring after severe traumatic brain injury, subarachnoid hemorrhage, intracranial hematoma, or stroke. Measurements and main results: Optic nerve sheath diameter was measured with a 7.5 MHz linear ultrasound probe. ICP was measured invasively via a parenchymal device. Simultaneous measurements were performed atleast once a day during the first 2 days after ICP insertion and in cases of acute changes. There was a significant relationship between ONSD and ICP (78 simultaneous measures, r = 0.71, P \ ). Changes in ICP were strongly correlated with changes in ONSD (39 measures, r = 0.73, P \ ). Enlarged ONSD was a suitable predictor of elevated ICP ([20 mmhg) (area under ROC curve = 0.91). When ONSD was less than 5.86 mm, the negative likehood ratio for raised ICP was Conclusion: In sedated neurocritical care patients, non-invasive sonographic measurements of ONSD are correlated with invasive ICP, and the probability to have raised ICP if ONSD is less than 5.86 mm is very low. This method could be used as a screening test when raised ICP is suspected. Keywords Ocular ultrasound Traumatic brain injury Subarachnoid hemorrhage Elevated intracranial pressure Optic nerve sheath Introduction In neurocritical care, the detection of raised intracranial pressure (ICP) remains crucial as it is associated with poor outcome [1, 2]. Invasive ventricular devices are the gold standard for continuous and reliable measurement of ICP; however, their placement could be challenging due to blood coagulation disorder or lack of surgical availability [3]. Moreover, malfunction or obstruction of ventricular catheters has been reported to occur as often as 6% [4]. Non-invasive ocular ultrasonography has recently been proposed to detect elevated ICP. The retrobulbar segment of the optic nerve is surrounded by a distensible subarachnoid space which can inflate during increase in CSF pressure [5 10]. Optic nerve sheath measurement using ocular sonography has been performed since more than 10 years. Clinical studies have suggested that sonographic measurements of optic nerve sheath diameter (ONSD) correlates with clinical signs of high ICP in children with hydrocephalus or liver failure [10 13]. In adults with moderate traumatic brain injury (TBI), ONSD is also correlated with signs of high ICP on computed tomography (CT) [12, 14]. We recently published in the Journal the usefulness of sonographic measurement of ONSD for

2 2063 detecting raised ICP in the first 48 h after severe TBI, and found a significant relationship between ONSD and intraparenchymal ICP (r = 0.68) [15]; however, as highlighted in the editorial accompanying this article OSND was measured early after trauma, before ICP placement; it is therefore not really possible to determine the correlation between ICP and ONSD values, taken concurrently, and ICP is a dynamic parameter, which changes rapidly over time, and at the moment we do not know whether or how OSND would change according to subsequent ICP increases or decreases [16]. We therefore carried out this study in neurocritical care patients requiring invasive ICP insertion to determine the relationship between simultaneous measurements of sonographic ONSD and intraparenchymal ICP, with a particular attention to acute changes of ICP and ONSD. This work was presented in part at the 28th International Symposium on Intensive Care and Emergency Medicine in Brussels, Belgium, March 2008 [17]. Methods Study population Adult patients requiring sedation, mechanical ventilation, and ICP monitoring [severe traumatic brain injured patients with post-resuscitation Glasgow coma scale (GCS) score B 8, or patients with spontaneous subarachnoid hemorrhage, intracranial hematoma or stroke] were considered for inclusion from May 2007 to October Patients with ocular trauma, a known history of ocular pathology (as glaucoma or cataract) were excluded from the study. Patient care was inline with existing protocols and was not modified by this study. The study design was approved by the local research and ethics committee (Le Kremlin-Bicêtre, France). Given the observational nature of the study, the committee waived the requirement for informed consent from the patient or his (or her) family. All patients were sedated with midazolam and sufentanil administered intravenously during the study period. Injury severity score (ISS) and simplified acute physiology score (SAPS II) were calculated at day 1 after patient arrival [18, 19]. After a decision to place an ICP monitoring device (by the intensive care physician in charge), patients were enrolled in the study. ICP was measured via an intraparenchymal catheter (Neuromonitor-Microsensor kit Ò, Codman, Chatenay Malabry, France) inserted into the frontal lobe by a neurosurgeon. Fig. 1 Two-dimensional ocular sonography. Optic nerve sheath diameter (ONSD) and optic nerve diameter (OND) were measured 3 mm behind the globe, using an electronic caliper in an axis perpendicular to the optic nerve and according to previously described protocols [10, 12, 20 22]. The normal sonographic aspect of the optic nerve is from center to peripheral: hypoechogenic nerve fibers closely surrounded by the echogenic pia mater; the subarachnoid space appears anechogenic or hypoechogenic and is surrounded by hyperechogenic dura mater and periorbital fat [23]. The optic nerve diameter (OND) can be measured as the distance inside pia mater, and the ONSD as the distance inside dura mater. OND and ONSD were measured 3 mm behind the globe, using an electronic caliper and an axis perpendicular to the optic nerve (Fig. 1). For each optic nerve, two measurements were made: one in the sagittal plane and the other in the transverse plane, by rotating the probe clockwise. The mean of value obtained for both eye was retained as the OND and the ONSD values. Measurements of ONSD, OND, and ICP were performed at day 1 and 2 post-icp insertion. We were therefore able to collect for the same patient at least two simultaneous measures of ICP and ocular sonography. By calculating the difference between those paired-measures, the effects of ICP changes on ocular sonography can be described. Ocular sonography was also performed in case of acute changes in ICP (more than 15 mmhg) and investigator s availability. Ocular sonography Ultrasound examination of the eye was performed by investigators trained in ocular sonography (T.G. or S.M.) Hemodynamic and intracranial monitoring Arterial pressure was monitored continuously, via a femoral catheter (four French, Seldicath Ò, Plastimed,

3 2064 Saint Leu La Forêt, France). ICP reading was collected at the end of ocular sonography and CPP was calculated as the difference between mean arterial pressure (MAP) and ICP. Statistics After having checked that normal distribution cannot be rejected using Shapiro-Wilk test, linear regression was used to assess the correlation between ICP and sonographic measurements. Values of P \ 0.05 were considered significant. All values are expressed as mean ± SD, except for categorical data (median, range). Receiver operating characteristic (ROC) curves were plotted and areas under the curve (AUC) were estimated using the MedCalc Ò 9.1 Software (Belgium). Results Thirty-seven adult neurocritical patients requiring sedation and ICP monitoring were included. Twenty-two patients had severe TBI, six had subarachnoid hemorrhage, eight had intracranial hematoma and one had stroke. Demographic data are presented in Table 1. Seventy-eight simultaneous measurements of ICP, ONSD and OND were performed on these 37 patients. In 33 patients, two measures were performed (day 1 and 2, as planned) resulting in 66 measures (33 9 2). And in four patients, three measures were performed (two on day 1 and 2 as planned, and one additional measure related to acute change in ICP), resulting in 12 measures (4 9 3). Acute changes in ICP were related for one patient to important increase in ICP linked to brain death, and for three patients to an important decrease in ICP related to osmotherapy treatment (mannitol 20%, 250 ml). ICP and CPP The mean ICP among patients was 24.8 ± 16 mmhg, ranging from 3 to 77 mmhg. Thirty-eight ICPs were inferior or equal to 20 mmhg, and 40 were strictly superior to 20 mmhg. Mean CPP was 74 ± 20 mmhg, ranging from 5 to 117 mmhg and supported by norepinephrine to achieve therapeutic goals in 55% of cases. Ocular sonography Ocular sonography of both eyes was possible in all patients. The mean ONSD was 5.99 ± 0.40 mm, ranging from 5.33 to 7.08 mm. The mean OND was 4.53 ± 0.33 mm ranging from 3.63 to 5.53 mm. Correlation between ONSD and ICP A strong relationship was found between the mean ONSD and ICP (Fig. 2a; linear regression r = 0.71, P \ , 95% CI for regression coefficient = , 78 simultaneous measures). The 95% confidence limit for the prediction of ICP using ONSD was 20 mmhg. Changes in ONSD (delta) were also strongly related to ICP variations (39 simultaneous paired-measures, r = 0.73, P \ , 95% CI for regression coefficient = ) (Fig. 2b). A looser relationship was found between OND and ICP (Fig. 2c; linear regression, r = 0.28, P = 0.01, 95% CI for regression coefficient = ) and there was a very loose relationship between changes in ICP and changes in OND (Fig. 2d; 39 measures, r = 0.35, P = 0.03, 95% CI for regression coefficient = ). To check that the additional measures performed in cases of acute changes in ICP did not induce a bias related a single patient, we performed a per patient analysis by excluding these additional measures (n = 37 patients) and found a very similar relationship between ONSD and Table 1 Distribution of general and hemodynamic characteristics of patients Mean ± SD unless specified Range No. of patients 37 Age (years) 46 ± 17 [18 76] Weight (kg) 75 ± 11 [34 95] Sex (% of male) 70% Overall ICU length of stay (days) 23.9 ± 13 [5 54] SAPS II score 41 ± 12 [8 61] Injury severity score (if appropriate, n = 22) mode (range) 25 [9 76] Glasgow coma score, mode (range) 7 [3 15] MAP (mmhg) during sonography 98.9 ± 18 [65 157] ICP (mmhg) during sonography 24.8 ± 16 [3 77] CPP (mmhg) during sonography 74.1 ± 20 [5 117] Norepinephrine infusion during sonography (% of patients) 55% ICU intensive care unit, SAPS simplified acute physiology score, MAP mean arterial pressure, ICP intracranial pressure, CPP cerebral perfusion pressure

4 2065 Fig. 2 Relationship (linear regression line and 95% confidence interval in dotted lines) between intracranial pressure (ICP) and mean ultrasonographic optic nerve sheath diameter (ONSD) or optic nerve diameter (OND) (respectively, panel a and c). Relationships between changes (delta) in ICP and changes in ONSD or OND are presented, respectively, in panel b and d ICP (r = 0.71, P \ , 74 measures) and between changes in ONSD and changes in ICP (r = 0.74, P \ , 37 paired-measures). Detection of raised ICP by ocular sonography Receiver operating characteristic curves for ICP [ 20 mmhg were drawn for ONSD and OND. ONSD accurately predicted elevated ICP (AUC = 0.91; 95% CI = , P = ), with a best cut-off value of 5.86 mm (sensitivity 95%, specificity 79%). The negative likelihood ratio for this cut-off was The negative predictive value for raised ICP was 100% when ONSD was inferior to 5.80 mm. A contrario, ONS did not accurately predicted raised ICP (AUC = 0.62, 95% CI = , P = 0.05). The area under the ROC curves for ONSD and OND were significantly different (P \ ; Fig. 3). Discussion Fig. 3 Receiver operating characteristic curves for intracranial pressure (ICP), mean optic nerve sheath diameter and mean optic nerve diameter with respect to high ICP (ICP [ 20 mmhg) Our results show that sonographic ONSD (but not OND) is strongly related to ICP. Changes in ONSD are also strongly related to changes in ICP. The measure of the distension of the sheath surrounding the optic nerve (but not of the nerve itself) could be used to detect elevated ICP in neuro-icu patients. These results, by measuring strictly simultaneously ICP and ONSD, confirm those from previous studies from our and other team [12, 14, 15]. The optic nerve, as part of the central nervous system, is surrounded by a subarachnoid space [5 7]. The intraorbital part of the subarachnoid space is distensible and can therefore inflate if pressure in CSF increases. To our knowledge, only one study has compared ONSD with invasive ICP which remains the gold standard [15]; however, these measures were not strictly simultaneous. In the present study,

5 2066 using a larger cohort of patients (n = 37) and measuring ONSD and ICP simultaneously, we found very similar results, for the ONSD cut-off for raised ICP (5.8 mm in the present study vs. 5.7 mm in our previous study), and a similarly good relationship between ONSD and ICP (r = 0.71 vs. r = 0.68). The negative likelihood ratio of this cut-off value was 0.06, showing a very low probability of having high ICP when ONSD was less than 5.8 mm. In addition, we observed that ONSD changes strongly correlate with ICP variations. In this study, we also measured the OND which can also be easily obtained using ocular sonography [23]. OND had however a poor relationship with ICP, and changes of ICP were not detected by changes of OND. The variation of ONSD during raised ICP cannot therefore be related to optic nerve dilatation (as during optic nerve edema), but to its sheath distension, probably due to the increase in CSF pressure surrounding the optic nerve. An important limitation of this study is the relatively small number of patients included (n = 37). A more clinically relevant relationship between ONSD and ICP could probably be achieved with a larger cohort of patients. The observed relationship between ICP and ONSD is statistically significant and strong; however, from an individual point of view, ICP prediction by ONSD measurement remains difficult as a large range of ICPs can be observed for the very similar ONSD. As unusual high values of ICP ([50 mmhg) can influence regression characteristic. We have performed the same analysis by excluding these outliers (seven measures excluded) and found in 71 simultaneous measures a regression coefficient of 0.63 between ICP and ONSD, P \ The fact that only four simultaneous measures of ICP and ONSD have been performed in case of acute changes in ICP is also to underline. A selection bias could have been induced by investigator s unavailability to perform ocular sonography in case of acute change in ICP. A lack of sonographic experience is also an obvious limitation to the use of ocular sonography. As described by Tayal et al. [14] the learning curve seems to be rapid, indeed an experienced sonologist needs as few as ten measurements and three abnormal scan to obtain adequate results, while for novice sonologists 25 scans may be needed. Another limitation of ocular ultrasound could be the possible inter-observer variations; however, using exactly the same sonographic equipment the interobserver variation was shown by our team to be less than 0.3 mm [15], which is very similar to those described by other teams [23, 24]. The authors of the present study strongly support the need of continuous invasive ICP measurement in neuro- ICU patients with suspected raised ICP and all existing guidelines for TBI management recommend to measure and monitor the absolute ICP values. The aim of this study was certainly not to show any superiority of ocular sonography versus invasive ICP; however, having a noninvasive estimation of the risk of raised ICP is of interest when invasive ICP is not available or contraindicated. Nearly 30% of severe TBI patients are indeed managed in Europe in non-specialized centers without neurosurgical facilities [25]. Moreover, raised ICP is not a rare occurrence in patients with liver encephalopathy or meningitis [26, 27]. Non-invasive technology for absolute ICP value measurement based on computer modeling of eye artery blood flow using two-depth Transcranial Doppler has been described [28]. This technique showed excellent prediction of ICP, but also needed specific equipment. The exact prediction of ICP is probably lower using ocular sonography; however, the measure of ONSD can be performed without specific sonograph, and using a very conventional probe, and has a good sensitivity and negative likelihood ratio for raised ICP. Ocular sonography could serve as a bedside and easy-to-use detection tool for raised ICP. Conclusion In sedated neurocritical care patients, there is a significant relationship between non-invasive sonographic ONSD and invasive ICP. Values of ONSD less than 5.8 mm are not likely to be associated with ICP above 20 mmhg. Moreover, changes in ONSD are also strongly related to ICP changes. Ocular sonography with ONSD measurement for detecting raised ICP probably needs further validation study in a larger cohort of patients using dynamic test; however, this non-invasive bedside monitoring is a promising method to assess the probability of raised ICP. Acknowledgment The authors wish to thank Dr Olivier Berges (Foundation Opthalmologique Adolphe de Rothschild, Paris, France) for helpful discussion on ocular sonography. References 1. Becker DP, Miller JD, Ward JD, Greenberg RP, Young HF, Sakalas R (1977) The outcome from severe head injury with early diagnosis and intensive management. J Neurosurg 47: Marshall LF, Smith RW, Shapiro HM (1979) The outcome with aggressive treatment in severe head injuries. Part II: acute and chronic barbiturate administration in the management of head injury. J Neurosurg 50: Ghajar J (2000) Traumatic brain injury. Lancet 356:

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