Title | Strain and Shear Wave Elastography in Diagnosis of Retrobulbar Neuritis |
Creator | Tevfik Oğurel, Veysel Burulday |
Affiliation | Departments of Ophthalmology (TO) and Radiology (VB), Kirikkale University Medical Faculty, Kirikkale, Turkey |
Abstract | Background: In the early stages of retrobulbar neuritis (RN), the optic disc appears normal on ophthalmoscopy. Therefore, the diagnosis of RN is usually made clinically. However, imaging tools are needed for precise diagnosis of RN, and usually MRI is used. In this study, we investigated the diagnostic performance of strain elastography (SE) and shear wave elastography (SWE) in patients with RN. Elastography is a new sonographic technique and a noninvasive ultrasound method for evaluating the elastic properties of tissues based on static compression: the elastographic techniques of SE compress the tissues axially, and SWE uses waves that are generated by transducers and interact with the tissue. Methods: The study included 40 eyes of 20 patients with sudden visual loss, who were diagnosed with RN. The eyes of the patients were divided into 2 groups: the eye with a diagnosis of RN was the group of RN eyes, and the healthy second eye was the group of control eyes. Ophthalmologic examination, orbital and brain MRI, SE, and SWE were performed. SE color mapping was divided into 3 types: blue-hardest tissue (Type 1), blue/green-hard tissue (Type 2), and green-intermediate tissue (Type 3). All patients were treated with high-dose corticosteroids. The measurements of SE and SWE were made immediately after diagnosis and 1 month after treatment. Results: The mean age of 11 male and 9 female patients was 38.3 ± 12.2 years. At the time of diagnosis, the mean shear wave values for the control eyes were 18.47 ± 7.26 kPa (kilopascals), and the mean shear wave values for the RN eyes were 37.21 ± 8.24 kPa. There was a statistically significant difference between the control and RN eyes at the time of diagnosis (P < 0.001). The mean shear wave value was 19.92 ± 4.77 kPa in the RN eyes after treatment. There was a statistically significant difference in values at the time of diagnosis and after treatment (P < 0.001). Strain types found in the RN eyes before treatment were Type 1 in 60% of eyes, Type 2 in 25%, and Type 3 in 15%; at the end of the treatment, Type 2 was observed in 25% of eyes and Type 3 in 75%, while Type 1 was not observed. Conclusions: SE and SWE may be important alternative diagnostic tools in the diagnosis of RN. |
OCR Text | Show Original Contribution Strain and Shear Wave Elastography in Diagnosis of Retrobulbar Neuritis Tevfik O gurel, MD, Veysel Burulday, MD Background: In the early stages of retrobulbar neuritis (RN), the optic disc appears normal on ophthalmoscopy. Therefore, the diagnosis of RN is usually made clinically. However, imaging tools are needed for precise diagnosis of RN, and usually MRI is used. In this study, we investigated the diagnostic performance of strain elastography (SE) and shear wave elastography (SWE) in patients with RN. Elastography is a new sonographic technique and a noninvasive ultrasound method for evaluating the elastic properties of tissues based on static compression: the elastographic techniques of SE compress the tissues axially, and SWE uses waves that are generated by transducers and interact with the tissue. Methods: The study included 40 eyes of 20 patients with sudden visual loss, who were diagnosed with RN. The eyes of the patients were divided into 2 groups: the eye with a diagnosis of RN was the group of RN eyes, and the healthy second eye was the group of control eyes. Ophthalmologic examination, orbital and brain MRI, SE, and SWE were performed. SE color mapping was divided into 3 types: bluehardest tissue (Type 1), blue/green-hard tissue (Type 2), and green-intermediate tissue (Type 3). All patients were treated with high-dose corticosteroids. The measurements of SE and SWE were made immediately after diagnosis and 1 month after treatment. Results: The mean age of 11 male and 9 female patients was 38.3 ± 12.2 years. At the time of diagnosis, the mean shear wave values for the control eyes were 18.47 ± 7.26 kPa (kilopascals), and the mean shear wave values for the RN eyes were 37.21 ± 8.24 kPa. There was a statistically significant difference between the control and RN eyes at the time of diagnosis (P , 0.001). The mean shear wave value was 19.92 ± 4.77 kPa in the RN eyes after treatment. There was a statistically significant difference in values at the time of diagnosis and after treatment (P , 0.001). Strain types found in the RN eyes before treatment were Type 1 in 60% of eyes, Type 2 in 25%, and Type 3 in 15%; at the end of the treatment, Type 2 was observed in Departments of Ophthalmology (TO) and Radiology (VB), Kirikkale University Medical Faculty, Kirikkale, Turkey. The authors report no conflicts of interest. Address correspondence to Tevfik O gurel, MD, Department of Ophthalmology, Kırıkkale University Medical Faculty, Kirikkale University Campus, Ankara Road 6. Km, Yahşihan, Kirikkale 71100, Turkey; E-mail: ogureltevfik@hotmail.com O gurel and Burulday: J Neuro-Ophthalmol 2020; 40: 169-173 25% of eyes and Type 3 in 75%, while Type 1 was not observed. Conclusions: SE and SWE may be important alternative diagnostic tools in the diagnosis of RN. Journal of Neuro-Ophthalmology 2020;40:169-173 doi: 10.1097/WNO.0000000000000793 © 2019 by North American Neuro-Ophthalmology Society R etrobulbar neuritis (RN) is a form of optic neuritis (ON) characterized by inflammation of the optic nerve section at the back of the eye without ophthalmoscopic manifestations in the fundus (1). Patients present with subacute unilateral loss of vision and impaired color vision. Its etiology is demyelinating, inflammatory, or idiopathic, which may be acute or chronic (2). RN can be associated with a variety of conditions, particularly multiple sclerosis (MS) (1,3). Vision loss can be minimal, or the disease can result in severe visual loss (4). The type of therapy depends on the suspected cause of the problem. Steroid medications are widely used in the treatment of RN to reduce inflammation in the optic nerve. These are typically administered systemically. The optic disc may appear normal in the early ophthalmoscopic examination of RN. Therefore, the diagnosis of RN is usually made clinically. Clinical presentation usually includes some symptoms and findings such as partial vision loss or blurred vision, impaired color vision, relative afferent pupillary defect, and scotoma in the visual field. However, imaging tools are needed for the precise diagnosis of RN, especially in atypical presentation. MRI is the most important tool to image the retrobulbar area, which includes the optic nerve (5). Computerized tomography has limited applications in retrobulbar pathologies such as infection, inflammation, and neoplastic diseases because it uses ionizing radiation. While MRI offers high-resolution images, it is time consuming, costs more than other techniques, and often requires the use of gadolinium contrast. A more practical 169 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution method is needed to evaluate the retrobulbar area for the initial diagnosis and follow-up of patients (6). Elastography is a new sonographic technique and a noninvasive ultrasound (US) method for evaluating the elastic properties of tissues based on static compression: the elastographic techniques of strain elastography (SE) compress the tissues axially, and shear wave elastography (SWE) uses waves that are generated by transducers and interact with the tissue (7). In this study, we evaluated the optic nerve findings and diagnostic performance of SE and SWE; these techniques could become alternatives to MRI for patients with RN. METHODS The study was conducted with the permission of the Ethical Committee of the Kırıkkale University, with the informed consent of all patients concerned and in keeping with the Helsinki Declaration. Patients The study included 40 eyes of 20 patients with sudden visual loss in 1 eye; the patients were diagnosed with RN based on the criteria described by the Optic Neuritis Study Group (8). Patients' fellow healthy eyes were used as the control eyes. Inclusion criteria were acute RN of unknown or demyelinating etiology in patients aged 18 years or older. Exclusion criteria were glaucoma, use of a drug use that may affect the optic nerve, pseudotumor cerebri, systemic disease other than MS that might be the cause of the ON or other relevant retinal and/or optic nerve disease, such as ischemic, toxic, hereditary, and metabolic optic neuropathy, and follow-up period less than 1 month. The eyes of the patients were divided into 2 groups: the eye with a diagnosis of RN was the group of RN eyes and the healthy fellow eyes served as the group of control eyes. All control eyes appeared normal according to funduscopic examination, optic coherence tomography (OCT), and visual field testing. Ophthalmologic examination, visual field testing, OCT, SE, and SWE were performed before and 1 month after treatment. All patients received intravenous methylprednisolone 250 mg/6 hours (in 150 mL 5% dextrose solution) delivered over 1.5-2 hours for 3 days, followed by oral prednisolone for 11 days. All patients had a brain MRI. B-Mode Ultrasonographic and Elastographic Evaluation The B-mode and elastographic evaluations were made using a digital sonography unit with real-time tissue elastography software (LOGIQ E9; GE Healthcare, 2014, Wauwatosa, WI). The B-mode and SE images were obtained with a 6-15 D (4-15 MHz) multifrequency linear probe, and 170 SWE images were obtained with a 9L-D (2-8 MHz) multifrequency linear probe. The examination was performed with subjects in the supine position with eyes closed. After gel was applied to the eyelids, images were performed in the axial plane when both eyes were in neutral position. SE was performed applying light and rhythmic compression to the probe. Color coding of the SE was superimposed on the B-mode images and shown on a monitor. Screen images showing ideal compression (5-7 bar pressure) were evaluated according to the compression bar scale of 1-7 units. Within the device memory, a digital recording was made of the SE examination for later analysis in video format. In the optic nerve SE examination, a rectangular regions of interest (ROI) was selected 3 mm posterior to the optic nerve head. The SE results were color mapped based on 3 types of optic nerve elasticity, as follows: Type 1 (hardest tissue), predominantly blue; Type 2 (hard tissue), predominantly blue/green; and Type 3 (intermediate tissue), predominantly green (9). In the examination of the optic nerve by SWE, the ROI was only the nerve. The optic nerve sheath diameter (ONSD) was measured 3 mm behind the globe between the external hypoechogenic borders using an axis perpendicular to the optic nerve with the eyes in a neutral state and the subject in a supine position. The SWE examination of each patient was applied in the axial plane without compression, and a single screen displayed B-mode and SWE images simultaneously. The SWE evaluation was recorded and stored for further analysis using the digital video format of the device. Optic nerve hardness was analyzed quantitatively and expressed as kilopascal (kPa). Three measurements of each optic nerve were taken in a circular ROI at 1.5- to 2.5mm intervals, and the mean values were calculated for use in the statistical analysis because of anisotropic structure of the optic nerve. Figs. 1, 2 show elastographic evaluations of RN eyes and healthy control eyes. The same radiologist applied all of the US examinations for all the patients, and another radiologist confirmed the findings. The radiologists were blind to the clinical information of the participants. Statistical Analysis Statistical analysis was completed using IBM SPSS Statistics for Windows (Version 20.0). The Kolmogorov-Smirnov test was used to test the normal distribution of the data. Paired ttests and 1-way analysis of variance were used to compare data between the groups of eyes. Pearson Chi‐Square test was used to compare categorical variable. A P value of less than 0.05 was used to indicate statistical significance. RESULTS The mean age of the 11 male and 9 female patients was 38.25 ± 12.23 years. Best-corrected visual acuities were 0.43 ± 0.38 LogMAR in the RN eyes and 20.13 ± 1.22 in the healthy eyes at the time of the diagnosis. Strain types found O gurel and Burulday: J Neuro-Ophthalmol 2020; 40: 169-173 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 1. Affected eye of a 34-year-old patient with retrobulbar optic neuritis. A. The optic nerve (before treatment) shows a blue color coding (Type 1) with strain elastography (arrows) and the shear wave elasticity value was measured as 41.11 kPa (B). C. The optic nerve (after treatment) shows a green color coding (Type 3) with strain elastography (arrows), and the shear wave elasticity value was measured as 19.03 kPa (D). in the RN eyes before treatment were Type 1 in 60% of eyes, Type 2 in 25%, and Type 3 in 15%. At the end of treatment, Type 1 was not observed, Type 2 was found in 25% of eyes, and Type 3 was found in 75% of eyes. The mean shear wave values in the RN eyes were 37.21 ± 8.24 kPa before treatment and 19.92 ± 4.77 kPa after treatment (Table 1). There was a statistically significant difference in shear wave values before and after treatment (P , 0.001). The mean shear wave values in the control eyes were 18.47 ± 7.26 kPa. In the control eyes, strain Type 3 was found in 90% of eyes and Type 2 in 10%, but Type 1 was not observed (Table 2). There was a statistically significant difference between the control and RN eyes at the time of diagnosis (P , 0.001). There was no correlation between elastography values and age (P = 0.5) or gender (P = 0.6) in normal eyes. DISCUSSION This study demonstrated that elastographic images are different in affected eyes with RN and unaffected eyes. Also, the images performed before and after treatment were different. The strain values for the optic nerve in affected eyes were higher at the time of diagnosis compared with unaffected eyes and also after treatment. We also found that the SWE values and SE types correlate well with those obtained by MRI. RN is usually diagnosed based on the patient's clinical profile and examination, with subsequent confirmation via MRI (10). Accurate diagnosis is critical in starting appropriate and prompt ophthalmologic and neurologic evaluation and management. Often, the treatment includes intravenous steroids with the goal of preserving long-term visual function. MRI is ideal for diagnosing and evaluating many conditions, but it has some limitations, including high cost, limited availability, long scan time, and a great deal of noise, which disturbs the subjects. It may be uncomfortable for some people because it can produce claustrophobia (11,12). US remains the modality of choice in imaging many conditions due to its availability, safety, and low cost. Recently, it has become an important adjuvant in the FIG. 2. Healthy fellow eye. A. The optic nerve shows a green color coding (Type 3) with strain elastography (arrows) and the shear wave elasticity value was measured as 13.67 kPa (B). O gurel and Burulday: J Neuro-Ophthalmol 2020; 40: 169-173 171 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 1. Shear wave elastography values and types of elasticity in strain elastography in eyes with retrobulbar neuritis before and after 1 month of steroid treatment SWE (kPA) Strain elastography Blue (Type 1) Blue-green (Type 2) Green, green-yellow-red (Type 3) Before Treatment After Treatment P Value 37.21 ± 8.24 19.92 ± 4.77 ,0.001 ,0.001 12 (60%) 5 (25%) 3 (15%) 0 (0%) 5 (15%) 15 (75%) kPA, kilopascal; SWE, shear wave elastography. evaluation of the optic nerve. Candeliere Merlicco et al evaluated the utility of transorbital ultrasonography (TOS) for optic nerve atrophy in MS. They compared 59 patients with 36 healthy subjects and found that the diameter of the optic nerve was smaller in patients than in control subjects (13). In another study, Bäuerle et al studied the reproducibility and accuracy of ONSD assessment 3 mm behind the papilla using US compared to MRI. They demonstrated that TOS showed reliable measurement accuracy and is suitable for longitudinal investigations of the ONSD (14). Optic nerve inflammatory changes increase cellularity; however, the optic nerve sheath limits expansion, resulting in greater tissue stiffness (15). Recently, sonoelastography and US tissue characterization have been applied to optic nerve studies with the potential of increasing the diagnostic capability of ultrasonography. Sonoelastography was first introduced in 1991 by Ophir (16) with his work on foam blocks and bacon slabs. Based largely on the work of Hans Oestriecher, who had studied the physics of vibration in soft tissue, sonoelastography can measure the stiffness of biological tissues (13,17). It has been historically used in the assessment of internal organ pathology, and more recently, its clinical application to optic nerve tissue has been a growing area of interest (18). The 2 most common forms of sonoelastography are SE and SWE. SE visualizes tissue deformation with compression applied by the examiner. SWE is produced by the transducer and obtains quantitative information on tissue elasticity. SWE depends less on the operator, is more reproducible, and provides quantitative results (15,19). Our study is unique in using SWE to examine patients with RN before and after treatment. Vural et al (6) evaluated of the optic nerve and retrobulbar orbital fat tissue with strain ratio elastography. In this study, 12 subjects with permanent vision loss due to glaucoma were evaluated with sonoelastography and B-mode ultrasonography. They found that retrobulbar fat tissue strain values were significantly higher than the respective values for the optic nerve, and the strain values of the retrobulbar fat tissue and optic nerve had a statisti_ et al cally significant correlation (6). In another study, Inal (20) evaluated the optic nerve using SE and SWE in patients with MS and healthy subjects, and they found a statistically significant difference between the elasticity patterns of healthy participants and MS patients. Also, SWE values were higher in MS patients than in healthy controls (20). So far, there is only 1 study that used ultrasonic elastography in patients with ON. In that study (15), all patients were examined using acoustic radiation force impulse imaging with virtual touch tissue imaging quantification. The authors evaluated 13 patients with unilateral ON and found significantly different ultrasonic elastography values in the affected eye and the normal eye. In our study, all patients had RN, and the most important difference in our study is that we evaluated all RN patients before and after treatment. Also, the optic nerve was evaluated both quantitatively and qualitatively using both SE and SWE. Availability, high reproducibility, low cost, and minimal inter- and intraobserver variabilities make the sonographic approach highly beneficial. Therefore, it can be more widely used as a follow-up tool. We conclude that elastography is a reliable method of diagnosing RN. Also, SE and SWE TABLE 2. Shear wave elastography values and types of elasticity in strain elastography in eyes with retrobulbar neuritis and fellow healthy control eyes SWE (kPA) Strain elastography Blue (Type 1) Blue-green (Type 2) Green, green-yellow-red (Type 3) Affected Eyes Control Eyes P Value 37.21 ± 8.24 18.47 ± 7.26 ,0.001 ,0.001 12 (60) 5 (25) 3 (15) 0 (0) 2 (10) 18 (90) kPA, kilopascal; SWE, shear wave elastography. 172 O gurel and Burulday: J Neuro-Ophthalmol 2020; 40: 169-173 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution may be accessible and important alternative diagnostic tools for evaluating RN before and after treatment. There are some important limitations to this study. First, the sample size was relatively small, and, second, it lacks a power analysis. Third, although the US and elastographic evaluations were performed by the same radiologists, who were experienced in US and elastography, the lack of intrarater and interrater reliability assessments should be stated as a limitation. CONCLUSIONS The findings of this study provide further evidence of the clinical usefulness of SE and SWE in the identification of RN. However, these findings warrant further investigation in larger prospective studies. STATEMENT OF AUTHORSHIP Category 1: a. Conception and design: T. O gurel; b. Acquisition of data: V. Burulday; c. Analysis and interpretation of data: T. O gurel and V. Burulday. Category 2: a. Drafting the manuscript: T. O gurel; b. Revising it for intellectual content: T. 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Date | 2020-06 |
Language | eng |
Format | application/pdf |
Type | Text |
Publication Type | Journal Article |
Source | Journal of Neuro-Ophthalmology, June 2020, Volume 40, Issue 2 |
Publisher | Lippincott, Williams & Wilkins |
Holding Institution | Spencer S. Eccles Health Sciences Library, University of Utah, 10 N 1900 E SLC, UT 84112-5890 |
Rights Management | © North American Neuro-Ophthalmology Society |
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Setname | ehsl_novel_jno |
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Reference URL | https://collections.lib.utah.edu/ark:/87278/s6x69bcf |