Abstract
Objectives
We aimed to quantitatively assess Evans index (EI) using ultrasonographic optic nerve sheath diameter (ONSD) measurements in supine and upright position in normal pressure hydrocephalus (NPH) patients.
Methods
Ultrasonographically ONSD was measured in a supine and upright position before and 4–5 days after the ventriculoperitoneal shunt surgery. The changes of the ONSD between supine and upright positions were calculated as ∆ONSD = sONSD-uONSD and as the variation ONSD_V = 100% × [(sONSD − uONSD)/sONSD]. Multiple linear regression analyses were conducted to assess associations between EI and the variation of ONSD. We derived the mathematical function to predict EI. Bland–Altman analysis was applied to evaluate the accuracy and precision of the EI prediction.
Results
Thirteen adult patients (mean age 61.8 ± 11.1 (SD) years; 6 (46%) female) undergone VP shunt implantation for NPH. The mean EI was 0.432 (95% CI, 0.393–0.471) preoperatively and 0.419 (95% CI, 0.373–0.466) postoperatively (p = 0.066). There is a decrease of the ONSD during positional changes from supine to upright position and pre- and postoperative EI correlated with preoperative variation ONSD_V1 (r = − 0.610 and − 0.648, p < 0.05). The mathematical function for preoperative EI estimation was EIpreop = 0.504 − 0.022 × ONSD_V1 + 0.101 × gender (M = 0; W = 1), (Durbin-Watson value = 1.94), and for postoperative was EIpostop = 0.487 − 0.022 × ONSD_V1 + 0.117 × gender; (Durbin-Watson value 2.23).
Conclusions
Ultrasonographic ONSD measurements in supine and upright position provide a potential method to quantify EI that can be conducted at the bedside.
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Abbreviations
- ∆ONSD:
-
sONSD–uONSD
- CSF:
-
Cerebrospinal fluid
- CT:
-
Computer tomography
- D-W:
-
Durbin-Watson statistic
- EI:
-
Evans index
- ETV:
-
Endoscopic third ventriculostomy
- ICP:
-
Intracranial pressure
- iNPH:
-
Idiopathic normal pressure hydrocephalus
- LCL:
-
Lower confidence limit
- LOA:
-
Limits of agreement
- MRI:
-
Magnetic resonance imaging
- NPH:
-
Normal pressure hydrocephalus
- ONSD:
-
Optic nerve sheath diameter
- ONSD_V:
-
Variation of ONSD
- ONSD_V1:
-
Preoperative variation of ONSD
- ONSD_V2:
-
Postoperative variation of ONSD
- SD:
-
Standard deviation
- SE:
-
Standard error
- sONSD:
-
ONSD in supine
- UCL:
-
Upper confidence limit
- uONSD:
-
ONSD in upright
- US:
-
Ultrasound system
- VP shunt:
-
Ventriculoperitoneal shunt
References
Adams RD, Fisher CM, Hakim S, Ojemann RG, Sweet WH (1965) Symptomatic occult hydrocephalus with “normal” cerebrospinal-fluid pressure. A treatable syndrome. N Engl J Med 273:117–126. https://doi.org/10.1056/NEJM196507152730301
Agerskov S, Wallin M, Hellström P, Ziegelitz D, Wikkelsö C, Tullberg M (2019) Absence of Disproportionately Enlarged Subarachnoid Space Hydrocephalus, a Sharp Callosal Angle, or Other Morphologic MRI Markers Should Not Be Used to Exclude Patients with Idiopathic Normal Pressure Hydrocephalus from Shunt Surgery. AJNR Am J Neuroradiol 40(1):74–79. https://doi.org/10.3174/ajnr.A5910
Alvi MA, Brown D, Yolcu Y et al (2021) Prevalence and trends in management of idiopathic normal pressure hydrocephalus in the United States: Insights from the national inpatient sample. World Neurosurg 145:e38–e52. https://doi.org/10.1016/j.wneu.2020.09.012
Bäuerle J, Schuchardt F, Schroeder L, Egger K, Weigel M, Harloff A (2013) Reproducibility and accuracy of optic nerve sheath diameter assessment using ultrasound compared to magnetic resonance imaging. BMC Neurol 13:187
Bhandari D, Udupi Bidkar P, Adinarayanan S, Narmadhalakshmi K, Srinivasan S (2019) Measurement of changes in optic nerve sheath diameter using ultrasound and computed tomography scan before and after the ventriculoperitoneal shunt surgery in patients with hydrocephalus-A prospective observational trial. Br J Neurosurg 33(2):125–130. https://doi.org/10.1080/02688697.2019.1576856
Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1:307–1026
Borgesen SE, Gjerris F (1992) The predictive value of conductance to outflow of cerebrospinal fluid in normal pressure hydrocephalus. Brain 105:65–86
Bradley WG (2016) Magnetic resonance imaging of normal pressure hydrocephalus. Semin Ultrasound CT MR 37(2):120–128. https://doi.org/10.1053/j.sult.2016.01.005
Choi SH, Min KT, Park EK, Kim MS, Jung JH, Kim H (2015) Ultrasonography of the optic nerve sheath to assess intracranial pressure changes after ventriculo-peritoneal shunt surgery in children with hydrocephalus: a prospective observational study. Anaesthesia 70(11):1268–1273. https://doi.org/10.1111/anae.13180
Damasceno BP (2015) Neuroimaging in normal pressure hydrocephalus. Dement Neuropsychol 9(4):350–355. https://doi.org/10.1590/1980-57642015DN94000350
Ertl M, Aigner R, Krost M et al (2017) Measuring changes in the optic nerve sheath diameter in patients with idiopathic normal-pressure hydrocephalus: a useful diagnostic supplement to spinal tap tests. Eur J Neurol 24(3):461–467. https://doi.org/10.1111/ene.13225
Evans WA (1942) An encephalographic ratio for estimating ventricular enlargement and cerebral atrophy. Arch Neurol Psychiatry 47:931–937
Fichtner J, Ulrich CT, Fung C et al (2019) Sonography of the optic nerve sheath diameter before and after microsurgical closure of a dural CSF fistula in patients with spontaneous intracranial hypotension - a consecutive cohort study. Cephalalgia 39(2):306–315. https://doi.org/10.1177/0333102418793640
Hansen HC, Helmke K (1997) Validation of the optic nerve sheath response to changing cerebrospinal fluid pressure: ultrasound findings during intrathecal infusion tests. J Neurosurg 87(1):4–40
Hebb AO, Cusimano MD (2001) Idiopathic normal pressure hydrocephalus: a systematic review of diagnosis and outcome. Neurosurgery 49(5):1166–84; discussion 1184–6. https://doi.org/10.1097/00006123-200111000-00028
Kim DH, Jun JS, Kim R (2018) Measurement of the optic nerve sheath diameter with magnetic resonance imaging and its association with eyeball diameter in healthy adults. J Clin Neurol 14(3):345–350. https://doi.org/10.3988/jcn.2018.14.3.345
Lochner P, Czosnyka M, Naldi A et al (2019) Optic nerve sheath diameter: present and future perspectives for neurologists and critical care physicians. Neurol Sci 40:2447–2457. https://doi.org/10.1007/s10072-019-04015-x
Lotan E, Damadian BE, Rusinek H et al (2021) Quantitative imaging features predict spinal tap response in normal pressure hydrocephalus. Neuroradiology. https://doi.org/10.1007/s00234-021-02782-z
Marmarou A, Young HF, Aygok GA (2007) Estimated incidence of normal pressure hydrocephalus and shunt outcome in patients residing in assisted-living and extended-care facilities. Neurosurg Focus 22(4):E1. https://doi.org/10.3171/foc.2007.22.4.2
Mori E, Ishikawa M, Kato T, Kazui H, Miyake H, Miyajima M, Nakajima M, Hashimoto M, Kuriyama N, Tokuda T, Ishii K, Kaijima M, Hirata Y, Saito M, Arai H; Japanese Society of Normal Pressure Hydrocephalus (2012) Guidelines for management of idiopathic normal pressure hydrocephalus: second edition. Neurol Med Chir (Tokyo) 52(11):775–809. https://doi.org/10.2176/nmc.52.775
Nakajima M, Yamada S, Miyajima M et al (2021) Guidelines for management of idiopathic normal pressure hydrocephalus (third edition): endorsed by the japanese society of normal pressure hydrocephalus. Neurol Med Chir (Tokyo) 61:63–97. https://doi.org/10.2176/nmc.st.2020-0292
Neikter J, Agerskov S, Hellström P et al (2020) Ventricular volume is more strongly associated with clinical improvement than the Evans index after shunting in idiopathic normal pressure hydrocephalus. AJNR Am J Neuroradiol 41(7):1187–1192. https://doi.org/10.3174/ajnr.A6620
Ng SE, Low AM, Tang KK, Chan YH, Kwok RK (2009) Value of quantitative MRI biomarkers (Evans’ index, aqueductal flow rate, and apparent diffusion coefficient) in idiopathic normal pressure hydrocephalus. J Magn Reson Imaging 30(4):708–715. https://doi.org/10.1002/jmri.21865
Ohle R, McIsaac SM, Woo MY, Perry JJ (2015) Sonography of the optic nerve sheath diameter for detection of raised intracranial pressure compared to computed tomography: A systematic review and meta-analysis. J Ultrasound Med 34(7):1285–1294. https://doi.org/10.7863/ultra.34.7.1285
Padayachy LC, Kilborn T, Carrara H, Figaji AA, Fieggen GA (2015) Change in optic nerve sheath diameter as a radiological marker of outcome from endoscopic third ventriculostomy in children. Childs Nerv Syst 31(5):721–728. https://doi.org/10.1007/s00381-015-2655-0
Qvarlander S, Sundström N, Malm J, Eklund A (2013) Postural effects on intracranial pressure: modeling and clinical evaluation. J Appl Physiol 115(10):1474–1480. https://doi.org/10.1152/japplphysiol.00711.20
Raftopoulos C, Deleval J, Chaskis C et al (1994) Cognitive recovery in idiopathic normal pressure hydrocephalus: a prospective study. Neurosurgery 35(3):397–404; discussion 404–5. https://doi.org/10.1227/00006123-199409000-00006.
Reinard K, Basheer A, Phillips S et al (2015) Simple and reproducible linear measurements to determine ventricular enlargement in adults. Surg Neurol Int 6:59. https://doi.org/10.4103/2152-7806.154777
Robba C, Santori G, Czosnyka M et al (2018) Optic nerve sheath diameter measured sonographically as non-invasive estimator of intracranial pressure: a systematic review and meta-analysis. Intensive Care Med 44(8):1284–1294. https://doi.org/10.1007/s00134-018-5305-7
Toma AK, Holl E, Kitchen ND, Watkins LD (2011) Evans’ index revisited: the need for an alternative in normal pressure hydrocephalus. Neurosurgery 68(4):939–944. https://doi.org/10.1227/NEU.0b013e318208f5e0
Toms DA (2006) The mechanical index, ultrasound practices, and the ALARA principle. J Ultrasound Med 25(4):560–1; author reply 561–2. https://doi.org/10.7863/jum.2006.25.4.560
Vaiman M, Abuita R, Bekerman I (2015) Optic nerve sheath diameters in healthy adults measured by computer tomography. Int J Ophthalmol 8(6):1240–1244. https://doi.org/10.3980/j.issn.2222-3959.2015.06.30
Wang LJ, Yao Y, Feng LS et al (2017) Noninvasive and quantitative intracranial pressure estimation using ultrasonographic measurement of optic nerve sheath diameter. Sci Rep 7:42063. https://doi.org/10.1038/srep42063
YokoyamaY YY, Kosugi K et al (2021) Effect of gravity on brain structure as indicated on upright computed tomography. Sci Rep 11:392. https://doi.org/10.1038/s41598-020-79695-z
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This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the local (Kaunas regional biomedical research) ethics committee (2019–09-09/BE-2–60). All participants gave their informed consent prior to their inclusion in the study.
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Key points
1. We derived the mathematical function to predict Evans index using ultrasonographic optic nerve sheath diameter (ONSD) measurement in supine and upright position.
2. We propose that ultrasonographic measurement of ONSD in two positions provides a potential tool for quantitative evaluation of Evans Index in NPH patients.
3. Combining the results of our study and the data from the literature, we can assume that ultrasonographic measurement of ONSD in two different positions can predict EI and could be used as a screening tool in suspected NPH patients. It could also be used as a simple and effective method for further evaluation of the function of VP shunt after the operation.
This article is part of the Topical Collection on CSF Circulation.
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Urbonas, M., Raskauskiene, N., Deltuva, V. et al. Quantitative Evans index estimation using ultrasonographic measurement of the optic nerve sheath diameter in supine and upright position. Acta Neurochir 164, 1755–1764 (2022). https://doi.org/10.1007/s00701-022-05234-6
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DOI: https://doi.org/10.1007/s00701-022-05234-6