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| ORIGINAL ARTICLE |
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| Year : 2015 | Volume
: 52
| Issue : 4 | Page : 249-253 |
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Diagnostic value of optical coherence tomography in patients with idiopathic intracranial hypertension
Dalia M Labib MD 1, Dalia H Abdel Raouf2
1 Department of Neurology, Cairo University, Cairo, Egypt
2 Department of Ophthalmology, Cairo University, Cairo, Egypt
| Date of Submission | 27-Apr-2015 |
| Date of Acceptance | 31-Jul-2015 |
| Date of Web Publication | 27-Nov-2015 |
Correspondence Address:
Dalia M Labib
Department of Neurology, Cairo University, Cairo, 12111
Egypt
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/1110-1083.170656
Background
Idiopathic intracranial hypertension (IIH) is characterized by raised intracranial pressure in the absence of space-occupying lesions or other known etiology. It mainly affects young obese women, and may cause visual loss due to secondary optic atrophy.
Objective
The aim of the study was to investigate optical coherence tomography (OCT) and perimetry changes in patients with IIH at admission and 6 months later and highlight the relationship between OCT changes and severity of visual dysfunction measured by automated perimetry.
Patients and methods
This study included 30 female patients with IIH. Cerebrospinal fluid opening pressure was recorded. Complete ophthalmic evaluation included assessment of best-corrected visual acuity, perimetry, and retinal nerve fiber layer (RNFL) and ganglion cell complex (GCC) thickness within 3-4 days of performing the lumbar puncture. Thirty age-matched healthy women underwent a similar ophthalmological evaluation.
Results
In IIH patients the initial RNFL thickness was significantly higher, whereas GCC was significantly lower than that of controls (P = 0.045 and 0.004, respectively). The value of intracranial pressure measured was found to be positively correlated with the stage of papilledema (r = 0.494, P = 0.000). The final recordings showed significant decrease in GCC and RNFL values (P = 0.000 and 0.002, respectively) and improvement in mean deviation (P = 0.003).
Conclusion
GCC and RNFL thickness abnormalities in IIH patients were quantitatively correlated with visual field sensitivity losses. OCT is an effective tool for quantifying parameters of optic nerve damage. Keywords: GCC, idiopathic intracranial hypertension, optical coherence tomography, perimetry, retinal nerve fiber layer
How to cite this article:
Labib DM, Abdel Raouf DH. Diagnostic value of optical coherence tomography in patients with idiopathic intracranial hypertension. Egypt J Neurol Psychiatry Neurosurg 2015;52:249-53 |
How to cite this URL:
Labib DM, Abdel Raouf DH. Diagnostic value of optical coherence tomography in patients with idiopathic intracranial hypertension. Egypt J Neurol Psychiatry Neurosurg [serial online] 2015 [cited 2023 Dec 10];52:249-53. Available from: http://www.ejnpn.eg.net/text.asp?2015/52/4/249/170656 |
| Introduction | |  |
Increased intracranial pressure (ICP) is called idiopathic intracranial hypertension (IIH) or pseudotumor cerebri when intracranial mass, obstructive hydrocephalus, intracranial infections, hypertensive encephalopathy, and cerebral venous sinus thrombosis are excluded [1] . Clinical symptoms include headache from increased intracranial tension, visual disturbances, pulsating tinnitus, eye pain, and diplopia. The presence of papilledema is the main sign of suspected disease, and its grade determines the overall treatment strategy. Secondary optic neuropathy in IIH may cause permanent visual loss, which can be seen in 25% of patients. Hence, it must be identified early and adequately treated to avoid blindness [2],[3],[4] . Perimetry is the current method for evaluation of the visual system in IIH patients [5] , but it can show this complication only in 58-87% of patients [6],[7] .
Optical coherence tomography (OCT) is a noninvasive imaging technique producing cross-sectional images of the retina that quantifies thickness of the peripapillary retinal nerve fiber layer (RNFL) and macular ganglion cell layer (GCL) in vivo. It becomes a valuable tool to identify and monitor peripapillary RNFL thickness in optic neuropathies [8],[9] . Moreover, changes in GCL (macular thickness) are an important parameter of quantitative optic nerve atrophy in different optic neuropathies. RNFL thickness can be a more reliable method for quantitating the papilledema compared with ophthalmoscopy alone, which is subjective and may reflect significant interobserver variability. OCT has been suggested as a tool for monitoring the amount of RNFL thickness in optic disc edema [9] and for evaluating macular thickness as a parameter of optic nerve damage in patients with IIH [10],[11] .
The aim of the study was to detect OCT and perimetry changes in patients with IIH on admission and 6 months later and to highlight the relationship between OCT changes and the severity of visual dysfunction as measured by perimetry.
| Patients and methods | | |
This case-control study included 30 female patients with IIH diagnosed according to the International Headache Society classification criteria B [12] . The patients were recruited from the Neurology Department of Kasr El-Ainy Hospital, Cairo University, Egypt, during the period from January 2013 to January 2014. Thirty age-matched women were included as the control group. Symptoms and signs of increased ICP were ruled out clinically and by fundus examination in the control group.
Inclusion criteria
The inclusion criteria comprised age 18 years or more, BMI less than 25, cerebrospinal fluid (CSF) opening pressure (ICP) 20 cmH 2 O or more, normal CSF composition, normal MRI and MR venography, normal neurological examination except for papilledema and horizontal diplopia [12] , and best-corrected visual acuity (BCVA) of at least 1.0 logMARs. The patient was excluded if there was suspicion of any eye disorder other than papilledema [13] .
The patients signed an informed consent form, and approval from Cairo University Hospitals Research Ethics Committee was obtained.
The patients were subjected to a complete neurological history and examination, and the following data were recorded: current IIH symptoms and CSF opening pressure (latest). Lumbar puncture was performed using an 18- or 20-G spinal needle and a manometer positioned at a 90° angle to the spine. The opening pressure was determined by means of a column manometer while the subject was placed in the left lateral decubitus position and as relaxed as possible. All lumbar punctures were performed by a single neurologist.
The patients underwent complete ophthalmic evaluation, including BCVA logMARs, biomicroscopy of the anterior and posterior segments, intraocular pressure measurement, and automated perimetry [Swedish Interactive Threshold Algorithm (SITA) standard 24-2 strategy, Humphrey Visual Field Analyzer; Carl Zeiss Meditec, Dublin, California, USA]. A SITA standard strategy, program 24-2, was used to decrease the duration of the exam. The outcome measures evaluated were mean deviation (MD; dB) and pattern of visual field loss [pattern standard deviation (PSD); dB].
The OCTs were performed on average 3-4 days after the lumber puncture (LP), using RTVue spectral-domain OCT (Optovue Inc., Fremont, California, USA). It is based on the new-generation Fourier-domain optical coherence technology. Two different protocols were used; the first was the macular map protocol, which allows fast macular scan for GCC measurement. It consists of 12 radial line scans (1024 A-scans per line) in a three-dimensional 6´6 mm area (2.0 s). The second was the peripapillary RNFL NHM4 protocol, which consists of 12 radial scans (452 A-scans per line) over 3.45-mm diameter centered on the optic disc. It has the advantage of eye tracking and signal noise reduction. All scans were performed by a single investigator with ambient lighting and without pupil dilation to ensure patient comfort. Magnification of images 400-800% with contrast enhancement allowed for proper and accurate layer delineation.
A 90-D lens biomicroscopic assessment of the grade of papilledema was made on the basis of the scheme proposed by Frisén [14] . Controls were subjected to the same examinations as those of the patients, with BCVA of at least 0.18 (logMARs).
Statistical analysis
The data were coded and entered using statistical package for the social science (SPSS, version 15 for Microsoft Windows; SPSS Inc., Chicago, Illinois, USA). The data were summarized using descriptive statistics: mean and SD for normally distributed quantitative variables and median and range for non-normally distributed quantitative variables. Numbers and percentages were used for qualitative values. Comparison between patients and controls was done using the Student t-test for independent samples. Follow-up data were recollected for the patient group after 6 months and compared with the initial data. Within-group comparison between early and late values was made using the paired t-test. Correlation between various variables was determined using Pearson's moment correlation equation for linear relation in normally distributed variables and Spearman's rank correlation equation for either non-normal variables or for those with nonlinear relation. A regression model was constructed to determine the amount of variation in the difference in RNFL that is associated or responsible for variation in MD change. P values less than 0.05 were considered statistically significant.
| Results | | |
This study enrolled 60 eyes from 30 Egyptian female IIH patients and 30 age-matched healthy female controls (one eye from each participant was included). In [Table 1] are summarized the demographic data and clinical parameters of the IIH patients at the first visit and of controls. | Table 1 Demographic and clinical parameters of idiopathic intracranial hypertension patients in the first visit and of controls
Click here to view |
There were statistically significant differences between IIH and controls during the first visit as regards MD (P = 0.0001), PSD (P = 0.0003), and RNFL (P = 0.45); on the other hand, there was a nonsignificantly lower GCC thickness compared with healthy controls (P = 0.064). As regards the initial average RNFL thickness, despite being significantly higher compared with controls it was higher than normal in 40% of cases, within normal in 32% of cases, and below normal in 28% of cases. Concerning the initial average GCC thickness, it was within normal in 65% of cases and below normal in 35% of cases. When analyzing the previous data we found that 85% of patients with decreased RNFL thickness also showed decreased GCC thickness, whereas 13% of patients with elevated RNFL thickness had associated decrease of GCC thickness. These results indicate that signs of optic neuropathy can be detected in more than half of the IIH patients.
The grade of papilledema was significantly correlated to the mean value of CSF opening pressure measured by LP (r = 0.494, P < 0.001) and to the mean initial average RNFL thickness (r = 0.68, P = 0.03) and was not correlated to the mean initial average GCC thickness (r = 0.73, P = 0.44). In contrast, it is noted that the mean value of CSF opening pressure was not correlated to the mean initial average RNFL thickness (P = 0.210) or to the mean initial average GCC (P = 0.337). Other variables including BCVA, MD, and PSD did not show this correlation either with grade of papilledema or with CSF opening pressure.
Six months after recording the initial data, another recording was taken of BCVA, RNFL, GCC, MD, and PSD, and we compared these data with the previous ones. The most significant decrease was in GCC value (P < 0.001), followed by RNFL (P = 0.002) and papilledema (P = 0.023). There was significant improvement in MD (P = 0.003). Other variables including PSD and visual acuity showed insignificant change after 6 months of follow-up (P > 0.05).
[Table 2] illustrates the correlation between baseline OCT parameters and final perimetry by the end of 6 months of follow-up of the IIH patients. We found a significant nonlinear correlation between initial peripapillary RNFL with final MD (r = −0.368, P = 0.004) and PSD (r = 0.359, P = 0.005). As regards initial GCC it showed significant linear correlation with final MD (r = 0.710, P = 0.000) as well as with final PSD (r = −0.450, P = 0.000) in IIH patients. | Table 2 Correlation between baseline optical coherence tomography parameters and final perimetry of idiopathic intracranial hypertension patients
Click here to view |
Regression analysis showed that for every 10 μm of mean RNFL thickness increase at baseline, there was a 0.56 dB worsening in MD; in contrast, for every 10 μm of mean GCC thickness decrease at baseline, there was a 0.9 dB worsening in MD at the last follow-up.
| Discussion | | |
In the present study, we found that IIH patients had statistically significantly higher baseline average RNFL thickness as well as PSD compared with controls. As regards GCC thickness and MD, both showed lower baseline values when compared with controls.
Similarly, in a previous study carried out on children with pseudotumor cerebri, the authors reported increased average RNFL thickness in patients compared with controls. Their mean average RNFL thickness (125.7 ± 29.6 μm) was lower than that in the present study (130.16 ± 46.4 μm), which may be due to milder baseline grade of papilledema (the median grade was 1.0 vs. 2.0 in the present study) [15] . In addition, Rebolleda and Muñoz-Negrete [16] carried out a case-control study in IIH patients with early papilledema. Their results agreed with ours concerning the RNFL thickness. They found that the mean average RNFL thickness of patients was significantly greater than that of controls (P = 0.000).
Our results were in accordance with the case-control study conducted by Skau et al. [17] in 2013 on 20 newly diagnosed IIH patients, 21 long-term IIH patients, and 20 healthy controls. Investigations included measurement of peripapillary RNFL thickness and total retinal thickness, automated visual field testing, and measurement of CSF opening pressure. They found that PSD was significantly increased and MD was significantly decreased in IIH patients as compared with healthy controls [17] . They reported greater perimetric sensitivity losses in eyes with more edema. Elevated tissue pressure within the optic nerve due to the increased CSF pressure transmitted through the optic nerve sheaths may explain perimetric loss in patients with papilledema.
The current study showed that the grade of papilledema significantly correlated with the average initial RNFL thickness but not with average initial GCC thickness, which may be attributed to the differences in disease severity or duration of the patients studied.
Our results were in agreement with a recent study that has shown a significant positive correlation between grades of papilledema and peripapillary RNFL and total retinal thickness [18] . Moreover, Vartin et al. [19] reported that total retinal thickness correlates better than peripapillary RNFL thickness with a mild papilledema grade.
In the current study, there was a significant positive correlation between the CSF opening pressure and the grade of papilledema and it was correlated neither with the mean initial average RNFL thickness nor with the mean initial average GCC. Prior reports found that the CSF opening pressure significantly correlated with the grade of papilledema and with the average peripapillary RNFL; the correlation was either weak [18] or strong [20] . The difference in the timing of OCT relative to the lumbar puncture may be attributed to the difference between studies. In the study by Heckman et al. [20] , LP was performed before OCT, as in our study. It is well known that there may be temporary improvement of IIH symptoms immediately after an LP; a postspinal tap headache suggests that the puncture can transiently lower the CSF pressure. Furthermore, there is evidence that the RNFL thickness can decrease after LP [21] .
As regards the follow up of patients with papilledema, there was no way to determine whether RNFL thickness is decreasing and whether patients are improving or are progressing to optic atrophy. Sometimes by the time papilledema resolves, axonal damage has already occurred but cannot be detected by an ophthalmoscope. As decrease in macular thickness indicated the presence of optic neuropathy independently of RNFL, when we analyzed our data we found that 85% of patients with decreased RNFL thickness also had decreased GCC thickness, whereas 13% of patients with elevated RNFL thickness had associated decreased GCC thickness. This finding can be attributed to early retrograde optic nerve damage. The data support the effective value of OCT in quantizing retinal ganglion cell damage even in the early phase of the disease; thus, the GCL thinning at baseline may be a risk factor for IIH. These data agree with those reported by Marzoli et al. [2] in their prospective observational study carried out on 38 consecutive IIH patients in 2013. Their percentages were similar to ours as regards association of changes in RNFL and GCC. They found that increased RNFL thickness was associated with reduced mean GCC thickness in 10% of cases, whereas decreased RNFL thickness was associated with decreased mean GCC thickness in 83% of IIH patients [2] . Our result contrasted with the findings of a recent study that reported that structural loss in the retina or optic nerve head was uncommon at baseline. That may be because they specifically selected newly diagnosed IIH patients with mild to moderate papilledema of Frisén grade 2-4 [22] .
Six months after recording every patient's data, another recording was taken of visual acuity, RNFL, GCC, MD, and PSD, and we compared these data with the previous ones. The most significant decrease was in RNFL; on the other hand, there was significant improvement in the MD. Rebolleda and Muñoz-Negrete [16] observed similar findings concerning RNFL thickness, MD, and PSD in their study. There was significant decrease in RNFL thickness (P = 0.000), and the MD and mean PSD showed significant improvement (P = 0.000 and 0.005, respectively).
In the current study, when we evaluated the correlations between the initial RNFL thickness and the final MD and PSD (after 6 months) in our patients, we found that the mean average initial RNFL was inversely correlated with the final MD and directly correlated with final PSD. This goes with the results of previous studies that showed significant correlation between RNFL thickness and visual dysfunction [16],[23] . These data are in agreement with those of Rebolleda and Muñoz-Negrete [16] , who observed similar correlations between RNFL thickness and retinal sensitivity after 1-year follow-up in their study.
In this study regression analysis showed that for every 10 μm increase in initial mean RNFL thickness, there was a 0.56 dB worsening in MD, versus 0.6 dB worsening in the study by Rebolleda and Muñoz-Negrete [16] , and for every 10 μm decrease in initial mean GCC thickness there was a 0.9 dB worsening in MD at the last follow-up. These data plus the high significant correlation of the mean average GCC with the final MD and PSD indicate that the GCC thickness is a sensitive indicator for early retrograde optic nerve damage. In a recent study, the author reported that measurement of the GCL thickness shows promise of early detection of vision loss due to neuronal injury [22] . We agree with the findings of Skau et al. [9] that underestimation of RNFL thickness is suspected in cases of severe papilledema, and hence GCC thickness may present a more reliable parameter compared with RNFL alone.
In conclusion, our study confirms that OCT is a noninvasive, quantitative method of monitoring and following up papilledema in IIH patients, and it can show damage of ganglion cells in an early phase of IIH.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
| References | | |
| 1. | Wall M. Idiopathic intracranial hypertension (pseudotumor cerebri). Curr Neurol Neurosci Rep 2008; 8 :87-93.  |
| 2. | Marzoli SB, Ciasca P, Curone M, Cammarata G, Melzi L, Criscuoli A, et al. Quantitative analysis of optic nerve damage in idiopathic intracranial hypertension (IIH) at diagnosis. Neurol Sci 2013; 34 :S143-S145. |
| 3. | Dhungana S, Sharrack B, Woodroofe N. Idiopathic intracranial hypertension. Acta Neurol Scand 2010; 121 :71-82. |
| 4. | Ney JJ, Volpe NJ, Liu GT, et al. Functional visual loss in idiopathic intracranial hypertension. Ophthalmology 2009; 116 :1808-1813. |
| 5. | Wolf A, Hutcheson KA. Advances in evaluation and management of pediatric idiopathic intracranial hypertension. Curr Opin Ophthalmol 2008; 19 :391-397. |
| 6. | Rowe FJ, Sarkies NJ. Assessment of visual function in idiopathic intracranial hypertension: a prospective study. Eye 1998; 12 :111-118. |
| 7. | Liu IH, Wang AG, Yen MY. Idiopathic intracranial hypertension: clinical features in Chinese patients. Jpn J Ophthalmol 2011; 55 :138-142. |
| 8. | Huang-Link YM, Al-Hawasi A, Oberwahrenbrock T, Jin YP. OCT measurements of optic nerve head changes in idiopathic intracranial hypertension. Clin Neurol Neurosurg 2015; 130 :122-127. |
| 9. | Skau M, Milea D, Sander B, Wegener M, Jensen R. OCT for optic disc evaluation in idiopathic intracranial hypertension. Graefes Arch Clin Exp Ophthalmol 2011; 249 :723-730. |
| 10. | Rebolleda G, Muñoz-Negrete FJ. Follow-up of mild papilledema in idiopathic intracranial hypertension with optical coherence tomography. Vis Sci 2009; 50 :5197-5200. |
| 11. | Karam EZ, Hedges TR. Optical coherence tomography of the retinal nerve fibre layer in mold papilledema and pseudopapilloedema. Br J Ophthalmol 2005; 89 :294-298. |
| 12. | Headache Classification Subcommittee of the International Headache Society. The International Classification of Headache Disorders, 2nd edition. Cephalalgia 2004; 24 :9-160. [ PUBMED] |
| 13. | Randhawa S, Van Stavern GP. Idiopathic intracranial hypertension (pseudotumor cerebri). Curr Opin Ophthalmol 2008; 19 :445-453. |
| 14. | Frisén L. Swelling of the optic nerve head: a staging scheme. J Neurol Neurosurg Psychiatry 1982; 45 :13-18. |
| 15. | El-Dairi MA, Holgado S, O′Donnell T, Buckley EG, Asrani S, Freedman SF. Optical coherence tomography as a tool for monitoring pediatric pseudotumor cerebri. J AAPOS 2007; 11 :564-570. |
| 16. | Rebolleda G, Muñoz-Negrete FJ. Follow-up of mild papilledema in idiopathic intracranial hypertension with optical coherence tomography. Invest Ophthalmol Vis Sci 2009; 50 :5179-5200. |
| 17. | Skau M, Yri H, Sander B, Gerds TA, Milea D, Jensen R. Diagnostic value of optical coherence tomography for intracranial pressure in idiopathic intracranial hypertension. Graefes Arch Clin Exp Ophthalmol 2013; 251 :567-574. |
| 18. | OCT Sub-Study Committee for NORDIC Idiopathic Intracranial Hypertension Study Group, Auinger P, Durbin M, Feldon S, Garvin M, Kardon R, et al. Baseline OCT measurements in the idiopathic intracranial hypertension treatment trial, part II: correlations and relationship to clinical features. Invest Ophthalmol Vis Sci 2014; 55 :8173-8179. [ PUBMED] |
| 19. | Vartin V, Nuyen A, Balmitgere T, Bernard M, Tilikete C, Vighetto A. Detection of mild papilledema using spectral domain optical coherence tomography. Br J Ophthalmol 2012; 96 :375-379. |
| 20. | Heckman J, Weber M, Junemann A, Neundorfer B, Mardin C. Laser scanning tomography of the optic nerve vs CSF opening pressure in idiopathic intracranial hypertension. Neurology 2004; 62 :1221-1223. |
| 21. | Kupersmith M, Sibony P, Mandel G, Durbin M, Kardon R. Optical coherence tomography of the swollen optic nerve head: deformation of the peripapillary RPE layer in papilledema. Invest Ophthalmol Vis Sci 2011; 52 :6558-6564. |
| 22. | Heidary G, Rizzo JF. Use of optical coherence tomography to evaluate papilledema and pseudopapilledema. Semin Ophthalmol 2010; 25 : 198-205. |
| 23. | Kardon R. Optical coherence tomography in papilledema: what am I missing? J Neuroophthalmol. 2014; 34:S10-S17. |
[Table 1], [Table 2]
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