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Show Original Contribution Section Editors: Clare Fraser, MD Susan Mollan, MD The Effect of Different Optic Nerve Sheath Diameter Measurements Using Ultrasound to Assess Intracranial Pressure in Patients With Acute Brain Injury Jun Tian, MD, Guo-Biao Wu, MM, Xiao-Bing Liu, MD, Zhi-Yong Wang, MD, Jian-Ying Guo, MD Background: Optic nerve sheath diameter (ONSD) is a promising, noninvasive invasive intracranial pressure (ICP) measurement method. This study aims to analyze the differences in ONSD between the left and right eyeballs and the differences in ultrasonic measurement between the transverse and sagittal planes. Methods: Data from a total of 50 eligible patients with various types of brain injury who were admitted to our hospital from May 2019 to June 2021 were analyzed. An ONSD assessment was then performed using Philips B-mode ultrasound, measuring ONSD 3 mm posterior to the eyeballs. The left and right ONSDs in the transverse and sagittal planes were measured. Intraparenchymal fiber optic sensors and catheters were inserted into the ventricles and connected to an external pressure transducer to measure ICP. Results: A total of 164 sonographic measurements of ONSD were performed in 50 patients with brain injury in a prospective observational study. Statistically significant differences were found in ONSD between the transverse and sagittal planes. The difference in the left ONSD between the transverse and sagittal planes was 0.007 ± 0.030 cm (P = 0.003). The Spearman rank correlation test showed that the correlation coefficient between ICP and left/right ONSD in the transverse/sagittal planes was 0.495 vs 0.546 and 0.559 vs 0.605, respectively. The results showed that the areas under the curve of ONSD in the transverse and sagittal planes were 0.843 and 0.805, respectively. Medcalc software was used to compare the areas under the receiver operator characteristic curve, and the results showed that ONSD in the sagittal plane is generally better than in the transverse plane (P = 0.0145). Department of Neurosurgery (JT), Shijiazhuang People’s Hospital, Shijiazhuang, Hebei, China; Department of Neurosurgery (G-BW), The Second Hospital of Hebei Medical University, Shijiazhuang, Hebei, China; and Departments of Neurosurgery (X-BL) and Critical Care Medicine (Z-YW, J-YG), The Third Hospital of Hebei Medical University, Shijiazhuang, Hebei, China. Supported by Department of Science and Technology Key Research and Development Plan People’s Livelihood Special Project of Hebei Provincial Project number 19277763D. The authors report no conflicts of interest. Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (www. jneuro-ophthalmology.com). Address correspondence to Jian-Ying Guo, MD, Department of Critical Care Medicine, The Third Hospital of Hebei Medical University, No. 139 Ziqiang Road, Shijiazhuang 050000, China; E-mail:jianyingguo1794@163.com Tian et al: J Neuro-Ophthalmol 2024; 44: 201-205 Conclusions: This study found that ONSD in the sagittal plane is superior to the transverse plane regarding the comprehensive efficacy of ICP, and unilateral measurement is sufficient. Journal of Neuro-Ophthalmology 2024;44:201–205 doi: 10.1097/WNO.0000000000001942 © 2023 by North American Neuro-Ophthalmology Society S evere raumatic brain injury, brain hemorrhage, cerebral aneurysm, brain tumors, intracranial infection, postoperative cardiopulmonary resuscitation, and many other diseases can lead to brain damage, which may result in the increase of intracranial pressure.1–3 The timely and accurate determination of intracranial pressure is key to clinical treatment that targets interventions such as dehydration or surgical decompression. The gold standard for intracranial pressure monitoring is invasive intracranial pressure (ICP), which requires a neurosurgeon to surgically implant a monitoring device using a pressure probe inserted into the intraventricular or parenchyma of the brain. This procedure is expensive and can lead to complications, such as bleeding and infection.4 Many studies have shown that the ultrasonic measurement of the optic nerve sheath diameter (ONSD) is a promising noninvasive ICP measurement method that can reflect intracranial pressure5,6 with high sensitivity and specificity, and it can also be used to guide clinical practice.7,8 However, the specific measurement method of ONSD has not been completely standardized, and there are certain differences in the methods adopted by different studies.6 In most studies, ONSD is measured at 3 mm behind the eyeball, but the method of measurement is different, for example, transverse or sagittal planes and unilateral or bilateral eyeballs. For example, Jeon’s 2017 study only adopted ONSD measurement in the transverse plane,9 whereas most studies do not indicate whether they used ONSD in the transverse or sagittal planes.10,11 There are few studies on how these measurements differ and whether they affect ONSD and ICP predictions, and no specific studies have been found that consider this purpose. Therefore, this study intends to focus on the differences in the left and right eyeballs and measure ONSD in the transverse and sagittal planes to make up for the gap in ONSD measurement method research. This will provide a more accurate measure201 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution ment method, improve the accuracy of predicting intracranial pressure, and be valuable for the diagnosis of intracranial pressure. METHODS Patients In a prospective observational study, eligible patients with various types of brain injury who were admitted to the Department of Intensive Care Medicine and Neurosurgery of the Third Hospital of Hebei Medical University from May 2019 to June 2021 were enrolled. The inclusion criteria were as follows: (1) aged 14 years and above and (2) a Glasgow Coma Scale score from 3 to 12. The exclusion criteria were as follows: patients with a known history of ophthalmic disease or optic nerve injury. The research proposal was approved by the Ethics Committee of the Third Hospital of Hebei Medical University K2019-010-1. Optic Nerve Sheath Diameter Assessment and Data Collection The ONSD assessment was performed by an operator experienced in ultrasound examination using Philips B-mode ultrasound with a probe frequency of 5–10 Hz. The patient was placed in the supine or 30° supine position, and the probe was covered with an ultrasound gel and carefully placed on the closed upper eyelid without applying pressure to the eye. Conscious patients had to maintain a neutral eye position. If necessary, measurements were conducted under sedation for restless or uncooperative patients. Next, ONSD was measured at 3 mm behind the eyeball in the transverse and sagittal planes, as shown in Figure 1. The ONSD measurements of each eyeball in the transverse and sagittal planes were measured 3 times, respectively, and the average value was taken. The ONSD of each eyeball was the mean value of the transverse and sagittal planes. Invasive Intracranial Pressure Monitoring Two invasive methods were used to detect ICP: an intraparenchymal fiber optic transducer (Camino Laboratories, Integra LifeSciences, Princeton, CA) and a catheter inserted into the brain ventricles, which was connected to an external pressure transducer (Codman, Johnson & Johnson Medical Ltd, New Brunswick, NJ). The instruments were operated by neurosurgeons with routine clinical practice in the operating room. ICM+ software (ICM, Cambridge, United Kingdom) was used to monitor the data collection and the real-time calculation of ICP values. Statistical Analysis The data were analyzed using SPSS 22.0 and expressed as the mean ± SD. A value of P , 0.05 was considered statistically significant. The Spearman rank correlation test was used to conduct correlation tests. The ONSD results in the transverse and sagittal planes were compared, and a receiver operating characteristic (ROC) curve analysis of ICP was performed. Medcalc 20.0 software was used to compare the areas under the ROC curve. RESULTS Baseline Study A total of 164 ultrasound measurements of ONSD were performed in 50 patients with brain injury, of which 78 were measured at 30° supine. The 50 patients, of whom 12 were women and 38 were men, had a mean age of 53.1 years and a median age of 54 years (14–79 years old). The mean body mass index was 24 ± 2.7, and 33 patients had undergone decompressive craniectomy. Of the patients, 20 cases were spontaneous brain hemorrhage, 9 cases were aneurysm, 11 cases were brain trauma, and 10 cases were other types of brain injury. The mean ICP was 17.14 ± 5.89 mm Hg, the median ICP was 17 mm Hg and 64 cases were ICP $20 mm Hg. FIG. 1. A. Method for obtaining optic nerve sheath diameter in transverse plane; (B) method for obtaining optic nerve sheath in sagittal plane; (C) ONSD was measured 3 mm behind the eyeball. ONSD, optic nerve sheath diameter. 202 Tian et al: J Neuro-Ophthalmol 2024; 44: 201-205 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 1. Measurement of optic nerve diameter LT LS RT RS L R M-T M-S N Minimum (mm) Maximum (mm) Mean (mm) SD (mm) 164 164 164 164 164 164 164 164 4.2 46 4.2 4.4 4.5 4.4 4.3 4.6 7.6 7.7 7.6 7.8 7.6 7.7 7.6 7.8 6.26 6.32 6.25 6.35 6.28 6.302 6.25 6.33 0.69 0.67 0.68 0.65 0.66 0.66 0.67 0.67 L, the mean left optic nerve sheath diameter (ONSD) of transverse and sagittal planes; LS, left ONSD in sagittal plane; LT, left ONSD in transverse plane; M-S, the mean ONSD in sagittal plane of left and right eyes; M-T, the mean ONSD in transverse plane of left and right eyes; R, the mean right ONSD of transverse and sagittal planes; RS, right ONSD in sagittal plane; RT, right ONSD in transverse plane. Optic Nerve Sheath Diameter Measurement The mean left ONSDs in the transverse and sagittal planes were 6.26 ± 0.69 mm and 6.32 ± 0.67 mm, respectively. The mean right ONSDs in the transverse and sagittal planes were 6.25 ± 0.68 mm and 6.35 ± 0.65 mm, respectively. The mean ONSD of the left eye was 6.28 ± 0.66 mm, and that of the right eye was 6.30 ± 0.66 mm, see Table 1. Comparison of Left and Right ONSDs in the Transverse and Sagittal Planes A paired t test showed that the difference between the ONSDs in the transverse and sagittal planes was statistically significant (0.07 ± 0.30 mm, P = 0.003, Table 2). The right ONSD in the sagittal plane was statistically significant compared with the transverse plane, with a difference of 0.10 ± 0.24 mm (P , 0.001, Table 2). There were no statistically significant differences between the left ONSD and right ONSD in the transverse and sagittal planes (P . 0.05, Table 2). There was no significant difference in the mean ONSDs between the left eye and right eye (P . 0.05, Table 2). In addition, there was no difference of measure- ment in the ONSD between the supine and 30° supine, as shown in Supplemental Digital Content (see Table S1, http://links.lww.com/WNO/A737). Correlation Analysis Between Elevated Intracranial Pressure and Optic Nerve Sheath Diameter Invasive intracranial pressure of $20 mm Hg was defined as high intracranial pressure. The Spearman rank correlation test showed that the correlation coefficients between ICP and left/right ONSD in the transverse/sagittal planes, respectively, were 0.495 vs 0.546 (left ONSD in the transverse plane vs sagittal plane) and 0.559 vs 0.605 (right ONSD in the transverse plane vs sagittal plane). The correlation between the ONSD measurement in the sagittal plane and high cranial pressure was higher than that of the measurement in the transverse plane. See Table 3. Receiver Operating Characteristic Curve Analysis Between Invasive Intracranial Pressure ONSD in the Transverse and Sagittal Planes It was found that the areas under the curve (AUCs) measured by ONSD in the sagittal plane, transverse plane, and the mean of the sagittal and transverse planes were 0.843, 0.805, and 0.831, respectively. The cut off for ONSD in the sagittal plane was 6.56 mm, and the corresponding sensitivity and specificity were 77.4% and 84.3%; the cut-off for ONSD in the transverse plane was 6.51 mm, and the corresponding sensitivity and specificity were 67.7% and 82.4%; and the cut-off for the mean ONSD of the sagittal and transverse planes was 6.51 mm, and the corresponding sensitivity and specificity were 71.1% and 84.3%. Medcalc software was used to compare the areas under the ROC curve, and the results showed that ONSD in the sagittal plane was generally better than ONSD in the transverse plane (P = 0.0145). Furthermore, ONSD in the sagittal plane was better than the mean ONSD of the sagittal and transverse planes, but not statistically significant (P = 0.1125). The results are shown in Figure 2. TABLE 2. Paired t test for comparison of left and right longitudinal diameter and transverse diameter of optic nerve sheath LT—LS RT—RS LT—RT LS—RS L—R 95% IC Difference (mm) SD (mm) Standard Error Lower Upper T df P 20.0689 20.1006 0.0037 20.028 20.0183 0.2959 0.2387 0.3087 0.3116 0.2453 0.00231 0.00186 0.00241 0.00243 0.00192 20.01145 20.01374 20.00439 20.00761 20.00561 20.00233 20.00638 0.00513 0.002 0.00195 22.982 25.397 0.152 21.153 20.955 163 163 163 163 163 0.003 0 0.88 0.251 0.341 L, the mean left optic nerve sheath diameter (ONSD) of transverse and sagittal planes; LS, left ONSD in sagittal plane; LT, left ONSD in transverse plane; R, the mean right ONSD of transverse and sagittal planes; RS, right ONSD in sagittal plane; RT, right ONSD in transverse plane. Tian et al: J Neuro-Ophthalmol 2024; 44: 201-205 203 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 3. Correlation analysis between elevated intracranial pressure and optic nerve sheath diameter LT LS RT RS Correlation coefficient 0.495 0.546 0.559 0.605 P ,0.001 ,0.001 ,0.001 ,0.001 LS, left optic nerve sheath diameter (ONSD) in sagittal plane; LT, left ONSD in transverse plane; RS, right ONSD in sagittal plane; RT, right ONSD in transverse plane. DISCUSSION Up to now, many articles have been published on the relationship between ONSD and intracranial pressure. Some studies use the mean ONSD of the sagittal and transverse planes12 and some use the transverse plane,13 but few studies use ONSD in the sagittal plane alone. Furthermore, there are few studies on different measurement methods. In 2019, Arias et al14 published an article on ONSD measurement in the sagittal and transverse planes. It showed that the mean ONSD in the transverse plane was 5.6 mm, and the mean in the sagittal plane was 5.7 mm. In this study, the mean values of the sagittal and transverse planes were 6.33 and 6.27 mm, respectively. Consistent with Arias et al, the ONSD in the sagittal plane was generally larger than that in the transverse plane, suggesting that the optic nerve sheath itself is not exactly circular. In the ROC curve analysis, it was also found that the area under the AUC curve of ONSD in the sagittal plane was 0.843, which is better than 0.805 of the transverse plane and 0.831 of the mean of the sagittal and transverse planes. The cut-off for ONSD in the sagittal plane was 6.56 mm, and the corresponding sensitivity and specificity were 77.4% and 84.3%, respectively, which are better than in the transverse plane. These findings suggest that measuring ONSD in the sagittal plane may be a better choice in a clinical evaluation of intracranial pressure. However, these results are inconsistent with those of Arias et al, whose results show that ONSD in the sagittal plane has a narrower range of variability, whereas ONSD in the transverse plane has a better area under the ROC curve. In the study by Arias et al, the mean ONSD in the sagittal plane was 5.7 mm, and decompression was only 10%; however, the mean ONSD in the sagittal plane was 6.33 mm, and the ratio of decompression was 66% in this study, which reflected the different levels of intracranial pressure and severity of the patients included in this study. This may be one explanation for the different results, but further research is needed. In this study, there was no significant statistical difference between the left and right ONSD in sagittal and transverse planes, suggesting that the ONSD measurement of the left and right eyes was consistent. In 2018, Kavi et al15 studied ONSD diameter using computed tomography and measured ONSD at 3 mm, 6 mm, and 9 mm behind the eyeball. They found no major difference in 204 ONSD between the left and right eyeballs. In 2020, Andrea Naldi et al16 studied the asymmetry of bilateral ONSD in healthy people and patients with elevated intracranial pressure and found that the median diversity was higher in patients with intracranial hypertension than in healthy subjects (0.45 mm vs 0.23 mm) according to Welch t test using R software. The authors also failed to provide a reasonable explanation for such results, and it cannot be ruled out that the results are related to the special statistical method used, and no other studies have used similar methods. In addition, from the perspective of pathophysiology, it is still believed that subarachnoid space is interconnected, meaning that, theoretically, both sides should be symmetrical. In clinical practice, it is often impossible to measure the eyeball on a specific side because of trauma and other problems. Based on this study, measuring the eyeball on the opposite side can also represent the ONSD value of the eyeball. More than half of the cases included in this study had spontaneous intracerebral hemorrhage and craniocerebral trauma, and 33 patients (66%) underwent decompression with bone flap removal. The degree of damage in the left and right brain tissues in these patients is often different, and there is no relevant study to clarify whether the intracranial pressure on both sides is consistent for these patients. In this study, according to the ONSD values of the 2 eyeballs, it can be inferred that the intracranial pressure on both sides of such patients is consistent. Therefore, clinical measurement of ONSD in one eye can represent the overall FIG. 2. ROC curve analysis between invasive ICP and ONSD in the transverse and sagittal planes. MS: the mean ONSD in sagittal plane of left and right eyes; MT: the mean ONSD in transverse plane of left and right eyes, M: the mean ONSD of the transverse and sagittal planes. ICP indicates invasive intracranial pressure; ONSD, optic nerve sheath diameter; ROC, receiver operating characteristic. Tian et al: J Neuro-Ophthalmol 2024; 44: 201-205 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution ONSD level, which will significantly reduce the clinical workload and speed up clinical judgment. Because the accuracy of ultrasonic measurement relies on the skill and proficiency of the operator, there are sometimes measurement deviations caused by operators. Therefore, these research data come from the same operator to reduce the chance of error. Cimilli Ozturk et al17 evaluated the operator variations in the measurement of ONSD and found that the level of compatibility for most of the measurements was statistically acceptable. The authors concluded that it is hard to say that sonographic measurement of the ONSD is a highly reliable method both in the transverse and sagittal planes. Therefore, the possible differences in the details of ultrasonic technology led to a great difference in the cut-off value of ONSD.6 The cut-off value in this study was 6.5 mm, which is slightly larger than that in other literature, which may be related to the fact that the posterior 3 mm of the eyeball was used for measurement, whereas the posterior 3 mm of the retina was used for measurement in many other studies.17 There are some limitations in this study. First, the results of this study are more suitable for patients with elevated intracranial pressure. The difference in ONSD measurements between the transverse and sagittal planes in patients with relatively normal intracranial pressure needs further study. In addition, an age-matched healthy control population was not included in this study. The inability to compare ONSD measurements in different planes between patients and healthy individuals is another limitation of this study. Furthermore, the patients have a wide age range from 14 to 79 years, and the stratification analysis of the effects of ageing was not performed in this study because of the limited sample size. To address this limitation, increasing the sample size in future studies is necessary to refine these findings. Conclusions This study found that ONSD in the sagittal plane is superior to the transverse plane regarding the comprehensive efficacy of ICP and unilateral measurement is sufficient. STATEMENT OF AUTHORSHIP Conception and design: J.-Y. Guo, G.-B. Wu, J. Tian; Acquisition of data: X.-B. Liu; Analysis and interpretation of data: Z.-Y. Wang, J.-Y. Guo. Drafting the manuscript: J. Tian, G.-B. Wu, X.-B. Liu, Z.-Y. Wang, J.-Y. Guo; Revising the manuscript for intellectual content: J. Tian, G.-B. Wu, X.-B. Liu, Z.-Y. Wang, J.-Y. Guo. Final approval of the completed manuscript: J. Tian, G.-B. Wu, X.-B. Liu, Z.-Y. Wang, J.-Y. Guo. Tian et al: J Neuro-Ophthalmol 2024; 44: 201-205 REFERENCES 1. Chen LM, Wang LJ, Hu Y, Jiang XH, Wang YZ, Xing YQ. Ultrasonic measurement of optic nerve sheath diameter: a non-invasive surrogate approach for dynamic, real-time evaluation of intracranial pressure. Br J Ophthalmol. 2019;103:437–441. 2. Jimenez Restrepo JN, León OJ, Quevedo Florez LA. Ocular ultrasonography: a useful instrument in patients with trauma brain injury in emergency service. Emerg Med Int. 2019;2019:9215853. 3. Fernando SM, Tran A, Cheng W, et al. Diagnosis of elevated intracranial pressure in critically ill adults: systematic review and meta-analysis. BMJ. 2019;366:l4225. 4. Munawar K, Khan MT, Hussain SW, et al. Optic nerve sheath diameter correlation with elevated intracranial pressure determined via ultrasound. Cureus. 2019;11:e4145. 5. Zoerle T, Caccioppola A, D’Angelo E, et al. Optic nerve sheath diameter is not related to intracranial pressure in subarachnoid hemorrhage patients. Neurocrit Care. 2020;33:491–498. 6. Robba C, Santori G, Czosnyka M, et al. Optic nerve sheath diameter measured sonographically as non-invasive estimator of intracranial pressure: a systematic review and metaanalysis. Intensive Care Med. 2018;44:1284–1294. 7. Robba C, Cardim D, Tajsic T, et al. Ultrasound non-invasive measurement of intracranial pressure in neurointensive care: a prospective observational study. PLoS Med. 2017;14:e1002356. 8. Robba C, Donnelly J, Cardim D, et al. Optic nerve sheath diameter ultrasonography at admission as a predictor of intracranial hypertension in traumatic brain injured patients: a prospective observational study. J Neurosurg. 2019;132:1279–1285. 9. Jeon JP, Lee SU, Kim SE, et al. Correlation of optic nerve sheath diameter with directly measured intracranial pressure in Korean adults using bedside ultrasonography. PLoS One. 2017;12:e0183170. 10. del Saz-Saucedo P, Redondo-González O, Mateu-Mateu Á, Huertas-Arroyo R, García-Ruiz R, Botia-Paniagua E. Sonographic assessment of the optic nerve sheath diameter in the diagnosis of idiopathic intracranial hypertension. J Neurol Sci. 2016;361:122–127. 11. Moretti R, Pizzi B. Optic nerve ultrasound for detection of intracranial hypertension in intracranial hemorrhage patients: confirmation of previous findings in a different patient population. J Neurosurg Anesthesiol. 2009;21:16–20. 12. Weidner N, Kretschmann J, Bomberg H, et al. Real-time evaluation of optic nerve sheath diameter (ONSD) in awake, spontaneously breathing patients. J Clin Med. 2021;10:3549. 13. Du J, Deng Y, Li H, et al. Ratio of optic nerve sheath diameter to eyeball transverse diameter by ultrasound can predict intracranial hypertension in traumatic brain injury patients: a prospective study. Neurocrit Care. 2020;32:478–485. 14. Arias AA, Berrio JD. Comparison of two techniques to measure optic nerve sheath diameter in patients at risk for increased intracranial pressure. Crit Care Med. 2019;47:e940. 15. Kavi T, Gupta A, Hunter K, Schreiber C, Shaikh H, Turtz AR. Optic nerve sheath diameter assessment in patients with intracranial pressure monitoring. Cureus. 2018;10:e3546. 16. Naldi A, Provero P, Vercelli A, et al. Optic nerve sheath diameter asymmetry in healthy subjects and patients with intracranial hypertension. Neurol Sci. 2020;41:329–333. 17. Cimilli Ozturk T, Demir H, Yorulmaz R, Ozdemir S, Isat G, Ecmel Onur O. Assessment of intra-interobserver reliability of the sonographic optic nerve sheath diameter measurement. Kaohsiung J Med Sci. 2015;31:432–436. 205 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. |
