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ORIGINAL ARTICLE
Year : 2020  |  Volume : 33  |  Issue : 2  |  Page : 588-592

Intraocular pressure, ganglion cell complex, and retinal nerve fiber layer changes by optical coherence tomography in pseudotumor cerebri


1 Department of Ophthalmology, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Ophthalmology, Zagazig University, Zagazig, Egypt

Date of Submission09-Sep-2019
Date of Decision06-Oct-2019
Date of Acceptance07-Oct-2019
Date of Web Publication27-Jun-2020

Correspondence Address:
Ismail A Ismail
Fakous, Sharkia
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mmj.mmj_287_19

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  Abstract 


Objectives
The purpose of this study was to evaluate the changes in retinal nerve fiber layer (RNFL) thickness measured by optical coherence tomography (OCT) in idiopathic intracranial hypertension or pseudotumor cerebri (PTC).
Patients and methods
This cross-sectional comparative study involved 50 patients with PTC (group I) and 50 age-matched and sex-matched normal persons as controls (group II). Retinal nerve fiber thickness is measured using OCT for all studied population and then recorded and collected to be statistically analyzed.
Results
Visual acuity and best-corrected visual acuity were measured in both groups. Comparison between both groups shows a statistically highly significant difference (P < 0.01). Both groups showed a statistically highly significant difference between both groups (P < 0.01) regarding intraocular pressure. Thickness of the RNFL in the studied groups according to OCT measures showed a statistically very highly significant difference between both groups (P < 0.001).
Conclusion
RNFL thickness measurements can provide important information regarding retinal axonal loss in patients with papilledema from PTC. Although axonal loss was documented in the chronic phase of papilledema, our findings, to be confirmed in future prospective studies, suggest a possible use of OCT during the treatment of PTC syndrome.

Keywords: ganglion cell layer, pseudotumor cerebri, retinal nerve fiber


How to cite this article:
Farahat HG, Marey HM, Zaky MA, Ismail IA. Intraocular pressure, ganglion cell complex, and retinal nerve fiber layer changes by optical coherence tomography in pseudotumor cerebri. Menoufia Med J 2020;33:588-92

How to cite this URL:
Farahat HG, Marey HM, Zaky MA, Ismail IA. Intraocular pressure, ganglion cell complex, and retinal nerve fiber layer changes by optical coherence tomography in pseudotumor cerebri. Menoufia Med J [serial online] 2020 [cited 2020 Oct 24];33:588-92. Available from: http://www.mmj.eg.net/text.asp?2020/33/2/588/287772




  Introduction Top


The major morbidity of idiopathic intracranial hypertension (IIH) is visual impairment, which can be progressive and insidious. Visual loss is often reversible if treatment is initiated in a timely manner but can be permanent in up to 40% of patients. The most common visual field (VF) defects are enlargement of the physiologic blind spot, nasal steps, and arcuate defects. If the disease remains untreated, the patient can develop severe irreversible VF constriction[1].

VF loss with decrease in visual acuity (VA) occurs with advancing optic nerve damage and can progress to blindness. However, some patients present to medical attention with decreased VA. These patients pose a difficult dilemma to the physician, because some may have fulminant IIH, where the vision loss is due to severe papilledema and optic neuropathy, while others have vision loss from outer retinal changes in the macula[2].

Earlier studies of eyes with significant optic nerve head (ONH) swelling showed that two-dimensional segmentation analysis failures are common when using the proprietary optical coherence tomography (OCT) algorithms for measuring the effects of swelling in the peripapillary retina via the retinal nerve fiber layer (RNFL) thickness with spectral domain (SD)-OCT and TRT with time-domain OCT[3].

In this study, we evaluated the changes in RNFL thickness measured by OCT in patients with pseudotumor cerebri (PTC) or IIH.


  Patients and Methods Top


Study setting

This cross-sectional, comparative study involved 50 patients with PTC (group I) and 50 age-matched and sex-matched normal persons as controls (group II). They are collected from the Ophthalmology and Neurology Departments, Faculty of Medicine, Menoufia and Zagazig University Hospitals during the period from October 2016 to December 2018.

Protocol approval by the ethics committee

Before the beginning of the study and in accordance with the local regulation followed, the protocol and all corresponding documents were declared for Ethical and Research approval by the Ophthalmology Department, Menoufia University.

Inclusion criteria

The age of patients ranged from 30 to 50 years. Both sexes were included in the study. The patient group had elevated cerebrospinal fluid opening intracranial pressure (ICP) more than 25 mmHg measured by lumbar puncture at the time of diagnosis. The patients must be able to understand instructions and provide informed consent.

Exclusion criteria

Patients with intracranial diseases other than cranial venous sinus thrombosis such as tumors, glaucomatous patients, patients with posterior segment disorders such as diabetic retinopathy, age-related macular degeneration, etc.; patients who had a history of any type of optic neuropathies such as inflammatory optic neuritis, history of ocular trauma, intraocular surgery, uncooperative patients, patients with bad compliance, and those who were unable to give informed consent.

Technical design

Best-corrected visual acuity was measured in Snellen and log MAR equivalent, intraocular pressure measurement using Applanation tonometer, anterior segment examination by slit lamp biomicroscopy, examination of the angle by Gonioscopy (Goldmann three-mirror lens), posterior segment examination by indirect ophthalmoscopy and slit lamp biomicroscopy with noncontact +90 D lens, color and fluorescein angiography (if possible). Fundus photographs were taken by using Topcon high-resolution Fundus Camera (Itabashi City, Tokyo, Japan) after injection of fluorescein dye into the brachial vein of the forearm.

OCT of both eyes: SD-OCT (Topcon 3 D, 2000, Itabashi City, Tokyo, Japan) score of both eyes was used to measure RNFL thickness and ganglion cell layer (GCL) thickness for all studied population and then recorded and collected to be statistically analyzed using both SPSS, version 22 medical statistical software (SPSS, SPSS Inc., Chicago, Illinois, USA) and Microsoft Excel, version 2013 (Microsoft company, Washington City, USA).

OCT is used to analyze RNFL in superior, inferior nasal, and temporal quadrant of peripapillary RNFL, cup-to-disk ratio, cup volume, and rim area with GCL in the macula. OCT based on low-coherence interferometry, typically employing near-infrared light, is used.


  Results Top


OCT is used to measure RNFL and GCL thicknesses to determine if their thickness is affected by disease IIH (PTC). This cross-sectional comparative study involved 50 patients with PTC (group I) and 50 age-matched and sex-matched normal persons as controls (group II) as shown in [Table 1].
Table 1: Demographic distribution of the studied groups

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Comparison between both groups shows a statistically highly significant difference (P < 0.01) as regards VA. The intracranial tension (ICT) showed a statistically nonsignificant difference between both groups [Table 2].
Table 2: Visual acuity and refractive errors of the studied groups

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Comparison between both groups shows a statistically nonsignificant difference (P > 0.05) as regards spherical error and there is a statistically significant difference as regards cylindrical error (P < 0.05) [Table 2].

There is a statistically significant difference comparing ICT in both the study groups (P < 0.05) [Table 3], while statistical analysis of the right and left ICP are shown in detail in [Table 3].
Table 3: Intracranial tension and intraocular pressure of the studied groups

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The study shows that there was a reduction in RNFL thickness in the IIH group compared with the control. There is a statistically very highly significant difference between both groups (P < 0.001). This indicates that there is a marked axonal loss of RNFL in the IIH group ([Table 4] and [Figure 1]) and the GCL thickness was found to be highly significant (P < 0.01) by comparing the two groups ([Table 4] and [Figure 2]).
Table 4: Retinal nerve fiber layer and ganglion cell layer thickness of the studied groups according to optical coherence tomography

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Figure 1: Mean retinal nerve fiber layer (RNFL) thickness (μm) in both eyes of the studied groups.

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Figure 2: Mean macular areas thickness of the studied groups according to OCT measures. OCT, optical coherence tomography.

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  Discussion Top


Optic neuropathy secondary to IIH may be a severe complication which must be early identified, adequately monitored, and treated to avoid blindness[4].

Clinical assessment of anterior visual pathway diseases involves both functional evaluations, such as VA and VF assessments, and structural evaluations of the neural elements of the eye, traditionally ONH appearance and, more recently, RNFL thickness and GCL thickness measurements[5].

OCT is associated with morphologic and metabolic changes in the brain, thus providing an easily accessible window into the brain in neurologic diseases[6].

The purpose of this study was therefore to evaluate the ability of OCT-measured RNFL and GCL thicknesses to estimate neural loss in the eyes of patients with PTC.

This study involved 50 patients with PTC representing group I and 50 patients representing the control group II; both groups were age and sex matched.

According to the sociodemographic data, [Table 1] shows that there was no significant differences between both groups as regards age and for the sex both groups were the same and the percentage of women (80%) were higher than men (20%).

As regards VA, [Table 2] shows a statistically highly significant difference (P < 0.01) between both groups in VA and best-corrected visual acuity.

In support of our study, the study by Chen et al.[7] found that 4.7% of patients with IIH referred to a tertiary center had decreased VA on presentation.

For refractive errors of the studied groups in [Table 3], there was a statistically nonsignificant difference (P > 0.05) as regards spherical error and there was a statistically significant difference as regards cylindrical error (P < 0.05).

[Table 4] shows a statistically significant difference between both groups in ICT.

In the study by Monteiro and Afonso[8] an increase in ICP was observed in PTC that matched our study.

For the intraocular pressure measured in both groups a mild increase was seen in intraocular pressure of the IIH group I compared with the control group II and there was a statistically significant difference between both groups (P < 0.05).

In the study by Salpietro and Ruggieri[9] an increase in intraocular pressure was observed in patients with IIH which also supports our study result.

The thickness of RNFL in the studied groups according to OCT measures is shown. There was an increase in thickness in the PTC group I compared with the control group II. There is a statistically very highly significant difference between both groups (P < 0.001) which indicated a marked axonal loss of RNFL in the PTC group.

Rizzo et al.[10] stated that the OCT data showed that the average RNFL thickness is also reduced by surgical intervention resulting in a reduction of average RNFL thickness.

The study by Skau et al.[11] investigated OCT in IIH using the RNFL thickness in a peripapillary ring scan as the outcome parameter. Parallel to our results, patients with newly diagnosed IIH presented RNFL thickening compared with healthy controls, which decreased after 3 months under IIH treatment, thus proposing RNFL thickness as a potential longitudinal measure. Consequently, the peripapillary RNFL thickness measurement is only a rough estimate of ONH changes as it is located at the marginal zone of the pathologic process[12].

Laemmer et al.[13] investigated 23 patients with IIH using scanning laser polarimetry (GD × VCC) and found, compared with normal participants, an increase in RNFL thickness in patients with papilledema and a decrease in RNFL in 10 out of 13 patients with regression of papilledema. The authors pointed out that even in patients with effective treatment and regression of papilledema, axonal loss can be detected by scanning laser polarimetry. As for OCT, while several studies have evaluated its ability to quantify optic disk edema, none have used it to estimate axonal loss following papilledema[3],[12].

In contrast to our study, Marzoli et al.[14] studied 20 patients (40 eyes) who underwent SD-OCT measurements and found that the peripapillary retinal nerve fiber layer thickness (PRNFLT) was normal in 12 (30%) eyes, increased in 16 (40%) eyes, and reduced 12 (30%) eyes. GCCT was normal in 26 (65%) eyes and decreased in 14 (35%) eyes.

Also, the study by Kaufhold et al.[12] stated that RNFL thickness differed between IIH patients and controls, although a few patients showed very high RNFL thickness values which counter our study.

For the GCL it was observed that GCL thickness showed a reduction in the PTC group than the control group. All macular areas had a statistically significant difference that indicated a retinal ganglion cell (RGC) loss in the PTC group.

As regards the correlation between ICT and RNFL thickness in group I, Fig. 1 shows an inverse (negative) correlation as there is an increase in ICT and a decrease in RNFL thickness. There was a statistically significant negative correlation (r = −0.483, P < 0.05) and Fig. 2 shows the correlation coefficient (r) between ICT and RNFL thickness in group II that revealed an inverse (negative) correlation as there is an increase in ICT and a decrease in RNFL thickness. There was statistically insignificant negative correlation (r=−0.2385, P > 0.05).

Studies undertaken by Swanson et al.[15] and Rizzo et al.[10] support our study in finding a negative correlation between ICT and RNFL thickness.

The most important limitation of many of the equipment used in the quantification of axonal loss in papilledema is the difficulties introduced by the presence of disk edema itself. As most devices quantify RNFL in terms of thickness, the presence of swollen nerve fibers due to axonal transport blockage in the papilledema can confound the results. Thus, a reduction in RNFL thickness measurements in a patient under treatment for IIH could be due to either a reduction in raised ICP (indicating an improvement of the condition) or axonal loss of RGC (indicating a worsening of the condition).

Also among the limitations of this study, limitation of the rationale of the present study is the presence of confounding factors when RNFL thickness measurements are used as an indicator of axonal loss in acute papilledema and the relatively small number of patients and there were no comparison between patients before and after treatment to study the effect of treatment on visual reversal.

The data confirm the use of SD-OCT imaging as a noninvasive quantitative tool for diagnosing and monitoring papilledema in IIH[16]. PRNFLT measurements by SD-OCT can be more reliable to quantitate the amount of papilledema that ophthalmoscopy alone which is subjective and may reflect significant interobserver variability[14].

Since MGCCT measurements indicated the presence of optic neuropathy independently of the PRNFLT ones, the data support the use of SD-OCT analysis to quantitate RGCs damage in an early phase of the disease[14].

In summary, our findings suggest ONH volume scans as a diagnostic and progression parameter in IIH with higher sensitivity to ICP changes than RNFL thickness. OCT is a fast and an inexpensive method[12].


  Conclusion Top


In summary, our findings suggest ONH volume scans as a diagnostic and progression parameter in IIH with higher sensitivity to ICP changes than RNFL thickness. OCT is a fast and inexpensive method for detection of intracranial hypertension.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Keltner JL, Johnson CA, Cello KE, Wall M. NORDIC Idiopathic Intracranial Hypertension Study Group. Baseline visual field findings in the Idiopathic Intracranial Hypertension Treatment Trial (IIHTT). Invest Ophthalmol Vis Sci 2014; 55 :3200–3207.  Back to cited text no. 1
    
2.
Mensah A, Milea D, Jensen R, Fledelius H. Persistent visual loss in malignant idiopathic intracranial hypertension. Acta Ophthalmol 2010; 87 :934–936.  Back to cited text no. 2
    
3.
Wang JK, Kardon RH, Kupersmith MJ, Garvin MK. Automated quantification of volumetric optic disc swelling in papilledema using spectral-domain optical coherence tomography. Invest Ophthalmol Vis Sci 2012; 53 :4069–4075.  Back to cited text no. 3
    
4.
Digre KB, Nakamoto BK, Warner JE, Langeberg WJ, Baggaley SK, Katz BJ. A comparison of idiopathic intracranial hypertension with and without papilledema. Headache 2009; 49 :185–193.  Back to cited text no. 4
    
5.
Monteiro ML, Cunha LP, Costa-Cunha LV, Maia OO, Oyamada MK. Relationship between optical coherence tomography, pattern electroretinogram and automated perimetry in eyes with temporal hemianopia from chiasmal compression. Invest Ophthalmol Vis Sci 2009; 50 :3535–3541.  Back to cited text no. 5
    
6.
Bassi ST, Mohana KP. Optical coherence tomography in papilledema and pseudopapilledema with and without optic nerve head drusen. Indian J Ophthalmol 2014; 62 :1146–1151.  Back to cited text no. 6
    
7.
Chen H, Chen X, Qiu Z, Xiang D, Chen W, Shi F, et al. Quantitative analysis of retinal layers' optical intensities on 3D optical coherence tomography for central retinal artery occlusion. Sci Rep 2015; 5 :9269.  Back to cited text no. 7
    
8.
Monteiro ML, Afonso CL. Macular thickness measurements with frequency domain-OCT for quantification of axonal loss in chronic papilledema from pseudotumor cerebri syndrome. Eye (Lond) 2014; 28 :390–398.  Back to cited text no. 8
    
9.
Salpietro V, Ruggieri M. Pseudotumor cerebri pathophysiology: the likely role of aldosterone. Headache 2014; 54 :1229.  Back to cited text no. 9
    
10.
Rizzo JL, Lam KV, Wall M, Wilson MD, Keltner JL. Perimetry, retinal nerve fiber layer thickness and papilledema grade after cerebrospinal fluid shunting in patients with idiopathic intracranial hypertension. J Neuroophthalmol 2015; 35 :22–25.  Back to cited text no. 10
    
11.
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.  Back to cited text no. 11
    
12.
Kaufhold F, Kadas EM, Schmidt C, Kunte H, Hoffmann J, Zimmermann H, et al. Optic nerve head quantification in idiopathic intracranial hypertension by spectral domain OCT. PLoS One 2012; 7 :e36965.  Back to cited text no. 12
    
13.
Laemmer R, Heckmann JG, Mardin CY, Schwab S, Laemmer AB. Detection of nerve fiber atrophy in apparently effectively treated papilledema in idiopathic intracranial hypertension. Graefes Arch Clin Exp Ophthalmol 2010; 248 :1787–1793.  Back to cited text no. 13
    
14.
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 :143–145.  Back to cited text no. 14
    
15.
Swanson JW, Aleman TS, Xu W. Evaluation of optical coherence tomography to detect elevated intracranial pressure in children. JAMA Ophthalmol 2017; 135 :320–328.  Back to cited text no. 15
    
16.
Wall M, George D. Idiopathic intracranial hypertension. A prospective study of 50 patients. Brain 1991; 114 :155–180.  Back to cited text no. 16
    


    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

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