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ORIGINAL ARTICLE
Year : 2020  |  Volume : 68  |  Issue : 3  |  Page : 636-639

Measurement of Choroid Thickness Using Optical Coherence Tomography to Monitor Intracranial Pressure in an Idiopathic Cranial Hypertension Model


1 Department of Ophthalmology, Yenikent State Hospital, Sakarya, Turkey
2 Department of Neurosurgery, Memorial Sisli Hospital, Istanbul, Turkey

Date of Web Publication6-Jul-2020

Correspondence Address:
Dr. Serdar Çevik
Memorial Şişli Hastanesi, Piyalepaşa bulvarı No: 4 34385, Şişli, İstanbul
Turkey
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0028-3886.288980

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 » Abstract 


Background: Idiopathic intracranial hypertension (IIH) is a condition with increased intracranial pressure (ICP) without mass lesion or a known etiology with normal cerebrospinal fluid (CSF) composition. With optical coherence tomography (OCT), which is a noninvasive imaging technique, cross-sectional scans of the retina, choroid, and optic nerve head can be obtained with a resolution that is close to histological resolution.
Aim: The study aimed to evaluate the efficacy of OCT in providing practical and sensitive measurements to follow-up patients with IIH.
Materials and Methods: This retrospective study included 22 patients with IIH and 22 healthy controls. OCT was used to measure peripapillary retinal nerve fiber layer thickness (RNFLT), ganglion cell layer (GCL) thickness and inner plexiform layer (IPL) thickness, and subfoveal choroidal thickness (CT). Lumbar puncture (LP) was performed to evaluate ICP. An association between subfoveal CT and ICP was noted in patients with IIH—a finding that has not been reported previously.
Results: Patients with IIH had increased RNFLT (P < 0.000) and CT (P < 0.000) compared with healthy controls. In addition, subfoveal CT was significantly correlated with ICP (rs= 0.851; P < 0.000).
Conclusion: Measurement of CT by OCT, which reflects ICP, allows for the follow-up of patients with IIH. In addition, it can be used to monitor other diseases with high ICP.


Keywords: Choroidal thickness, idiopathic intracranial hypertension, intracranial hypertension, optical coherence tomography
Key Messages: Idiopathic intracranial hypertension (IIH) is an increased intracranial pressure (ICP) condition that primarily affects young obese women. A noninvasive quantitative technique for monitoring ICP is not yet available. OCT is a noninvasive tool that can help to monitor IIH.


How to cite this article:
Ozdemir I, Çevik S. Measurement of Choroid Thickness Using Optical Coherence Tomography to Monitor Intracranial Pressure in an Idiopathic Cranial Hypertension Model. Neurol India 2020;68:636-9

How to cite this URL:
Ozdemir I, Çevik S. Measurement of Choroid Thickness Using Optical Coherence Tomography to Monitor Intracranial Pressure in an Idiopathic Cranial Hypertension Model. Neurol India [serial online] 2020 [cited 2020 Aug 10];68:636-9. Available from: http://www.neurologyindia.com/text.asp?2020/68/3/636/288980




Idiopathic intracranial hypertension (IIH) is a condition with increased intracranial pressure (ICP) without mass lesion or a known etiology with normal cerebrospinal fluid (CSF) composition.[1],[2] Increased ICP in IIH causes axoplasmic flow stasis and ischemia with or without papilledema.[3] Therefore, IIH may result in permanent vision loss, visual disturbance, and diplopia.[4] It primarily affects young obese females. With obesity being an epidemic, IIH has become a critical disease.[1]

IIH manifests as a headache, and diagnosis of moderate or severe IIH is simple. However, cranial imaging techniques are required to diagnose subclinical IIH. If symptoms such as headache, vision loss, or visual field loss are present, treatment is administered with the primary goal of decreasing ICP. ICP is usually assessed through lumbar puncture (LP), which is an invasive procedure. A noninvasive quantitative technique to monitor ICP is not yet available.

With optical coherence tomography (OCT), which is a noninvasive imaging technique, cross-sectional scans of the retina, choroid, and optic nerve head can be obtained with a resolution that is close to histological resolution. Spectral-domain OCT (SD-OCT) demonstrates retinal layers, such as the retinal nerve fiber layer (RNFL), and enables measurement of RNFL thickness (RNFLT) and choroid thickness (CT).[5] RNFLT, total retinal thickness, and optic disc volume reportedly increase in acute IIH,[6],[7] whereas RNFLT reportedly decreases in chronic IIH.[6],[8] In addition, a correlation among RNFLT, optic disc volume, and IIH severity has been observed.[6],[9],[10]

In this study, we hypothesized that CT measured using SD-OCT correlated with ICP. Therefore, OCT can be used as a noninvasive and quantitative technique to monitor patients with IIH.


 » Materials and Methods Top


This retrospective study included 22 patients (female, 20; male, 2) diagnosed with IIH as per the International Headache Society Classification Criteria B [2] in our hospital between 2014 and 2016. The study conformed to the tenets of the Declaration of Helsinki and was approved by the local ethics committee and informed consent was obtained from all patients and controls.

The study included patients who were aged >18 years and had high CSF opening pressure (ICP >25 cmH2O), normal cranial magnetic resonance imaging (MRI), normal CSF composition, and normal neurological examination barring papilledema and sixth abducens palsy. The exclusion criteria were as follows: history of any treatment for IIH or that affecting ICP; history of any ocular disorder that could influence the peripapillary RNFL, macular ganglion cell layer (GCL), or CT; and having a refractive disorder spherical equivalent ≥±4D and media opacity that can attenuate signal strength in OCT. In total, 22 healthy subjects recorded in OCT device from the outpatient clinic with similar age and body mass index (BMI) were enrolled in the control group. Controls who complained of symptoms such as headache, tinnitus, or visual discomfort suggestive of IIH were excluded. Any invasive procedure including LP was not applied to the controls.

Patients complaining of headache underwent a complete neurological examination, including direct ophthalmoscopy, performed by the same physician. LP was performed using standard 20-gauge spinal needles in patients who had no cranial MRI or neurological sign except papilledema and sixth nerve palsy. Opening pressure was measured in the lateral decubitus position with legs extended, and the head and spine placed in a flat position.

In the morning session before LP, the patients underwent a detailed ophthalmologic examination, including the measurement of best-corrected visual acuity on Snellen' chart, Ishihara color test, slit-lamp biomicroscopy, applanation tonometry, indirect ophthalmoscopy, optic disc photography, and SD-OCT. The examination was performed in all patients by the same opthalmologist.

SD-OCT was performed using the 3D OCT-2000 FA Plus Spectral Domain (Topcon Medical Systems, Inc. Tokyo, Japan), which has an 840-nm wavelength light source, 5-μm axial image resolution, and speed of 27,000 A-scans per se cond. Peripapillary RNFL scans were obtained using 3D optic disc protocol (6 × 6 mm, 512 × 128 voxels), which generates images from 128 horizontal linear scans performed by 512 A-scans in a 6 × 6 mm area around the optic disc. Peripapillary RNFLT was calculated automatically by the OCT device software [Figure 1]. CT was measured using a single 9-mm horizontal line scan through the fovea centralis with 1024 A-scan/B-scan captured 50 times in the same position and overlapped with 50 B-scan images by the OCT device software (9 mm × 0.15 mm, 1024 × 50 voxels). The enhanced choroidal mode was used to get a fine focus of the choroidal structure. B-scan images with low quality and indistinctive choroidal–scleral boundary were rejected. The eye that had a higher quality B-scan image was used for measurement. The B-scan scale was adjusted to 1:1 mm and image size was doubled up. CT was described as the vertical distance between the outer edge of the hyperreflective retinal pigment epithelium and the scleral boundary [Figure 2] and was manually measured at the fovea centralis by the same ophthalmologist using “built-in caliper” in the linear measurement tools of the OCT device software.
Figure 1: RNFLT was calculated automatically by OCT device software

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Figure 2: The choroid thickness was measured between the outer edge of the retinal epithelium and the boundary of sclera

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Data was statistically analyzed using the SPSS statistical package version 20.0 (SPSS Inc., Chicago, IL, USA). The Kolmogorov–Smirnov test was used to assess the normal distribution of age, BMI, peripapillary RNFLT, subfoveal CT, and ICP. Levene's test was used to assess the variance homogeneity of the variables. Mann-Whitney U test was used to compare the age, BMI, peripapillary RNFLT, and subfoveal CT between test and control groups. In addition, the relationship between the CT at the central fovea and ICP was assessed using the Spearman rank correlation test. The value of statistical significance was set at P < 0.05.


 » Results Top


This study comprised 22 patients (female, 20; male, 2) and 22 controls (female, 19; male, 3). The age range and mean age ± SD of patients was 19–48 years and 32.36 ± 7.82 years, respectively, whereas that of controls was 18–47 years and 30.09 ± 7.93 years, respectively. The average BMI of patients and controls was 32.14 ± 3.77 kg/m2 and 31.18 ± 4.73 kg/m2, respectively [Table 1].
Table 1: Demographic characteristics of study subjects

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The average of peripapillary RNFLT and subfoveal CT in patients was 121.68 μm: 258.22 μm (median, 118.50 μm: 248.50 μm), whereas it was 109.36 μm: 228.04 μm in the controls (median, 110 μm: 228 μm). Peripapillary RNFLT and subfoveal CT were both significantly increased in patients compared with controls (P < 0.000, z = −4.08; P < 0.000, z = −4.09, respectively) [Table 2]. [Figure 3] shows the subfoveal CT of both patients and controls. On [Figure 4], the patient numbered 18 was a 22-year-old female, complaining of headache and visual disturbance for about a month, who had severe papilledema and mild sixth nerve palsy with an opening ICP of 55 cmH2O and subfoveal CT of 348 μm. In addition, patient numbered 10 on [Figure 4] was a 37-year-old female, who had headache, visual disturbance, and severe papilledema with opening ICP of 50 cmH2O and subfoveal CT of 326 μm. ICP ranged from 27 cmH2O to 55 cmH2O (mean, 36.68 ± 10.10 cmH2O). Furthermore, ICP was positively correlated with subfoveal CT (rs= 0.851; P < 0.001) [Figure 4].
Table 2: Measurements of study subjects

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Figure 3: Subfoveal choroid thickness changes (control and patient)

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Figure 4: Correalation between the choroid thickness at the central fovea and CSF pressure

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 » Discussion Top


IIH predominantly affects young obese females, as observed in our study (female, 20; male, 2). IIH diagnosis requires an evaluation of patient history and papilledema severity. Direct or indirect funduscopy is the only way to assess papilledema severity. Although funduscopy is quick, repeatable, and inexpensive, it is mostly subjective and qualitative and depends on physician experience.

Increased ICP causes axoplasmic flow stasis because of axonal swelling at the level of the optic disc,[3] and it is shown as papilledema on funduscopy. In addition, peripapillary RNFLT can be increased and can be demonstrated and measured using SD-OCT. In this study, peripapillary RNFLT significantly increased, a result which is consistent with those of previous studies.[6],[11],[12] Axons of the GCL constitute the RNFL that lies along the inner side of the retina to form the optic nerve. Besides axonal swelling, increased perineural pressure from venous stasis may lead to capillary leakage and intraretinal fluid accumulation below the RNFL.

The choroid is formed by particularly vessels such as spleen and like a blood lake surrounding by retina and sclera. The ocular choroid has the highest vascular circulation in the human body, 10–20 times that of the cerebral cortex, while the retina is avascular. The choroid comprises blood vessels and soft connective tissue and is supplied with blood by the posterior ciliary arteries and drained by the posterior ciliary veins. In addition, the choroidal vessels are poorly autoregulated.[13],[14] An increased ICP may break down the venous drainage of the choroid, thereby affecting CT in patients with IIH. The current study observed a significantly increased CT in patients with IIH, which was significantly correlated with ICP. To our knowledge, OCT measurements of CT have not been previously applied in IIH. To date, papilledema severity was considered to be correlated with ICP in IIH.[6]

Papilledema development or peripapillary RNFL thickening can take hours or days. The choroid is soft tissue unlike the RNFL or other retinal layers that are dense. Therefore, ICP affects the choroid more easily than RNFL. In patients with chronic or long-term IIH, resolution of papilledema and axonal atrophy both result in RNFL thinning [6] despite an already high ICP. The current study comprised patients who had been newly diagnosed with IHH as well as those with long-term or chronic IIH. Therefore, the measurement of CT may be more beneficial than measurement of RNFLT in monitoring patients with chronic or long-term IHH.

Currently, LP is the only quantitative technique available to monitor ICP. However, it is an invasive and painful procedure that is not always clinically applicable. Even though both CT and RNFLT may be weak parameters in diagnosing IIH, they can undoubtedly indicate ICP alteration above the normal limits.


 » Conclusion Top


OCT is a noninvasive imaging technique, which can be used to measure CT to accurately predict ICP above normal limits. In an IIH study model, if ICP alteration above normal limits can be determined as a constant value in other neurological diseases, then CT can prove beneficial in monitoring ICP. Nonetheless, the small sample size and unknown interval disease were limiting factors of the present study.[15]

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patients have given their consent for their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
 » References Top

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Wall M. Idiopathic intracranial hypertension. Neurol Clin 2010;28:593-617.  Back to cited text no. 1
    
2.
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3.
Tso MO, Hayreh SS. Optic disc edema in raised intracranial pressure. IV. Axoplasmic transport in experimental papilledema. Arch Ophthalmol 1977;95:1458-62.  Back to cited text no. 3
    
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Ball AK, Clarke CE. Idiopathic intracranial hypertension. Lancet Neurol 2006;5:433-42.  Back to cited text no. 4
    
5.
Huang D, Swanson EA, Lin CP, Schuman JS, Stinson WG, Chang W, et al. Optical coherence tomography. Science 1991;254:1178-81.  Back to cited text no. 5
    
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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;251:567-74.  Back to cited text no. 6
    
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Skau M, Sander B, Milea D, Jensen R. Disease activity in idiopathic intracranial hypertension: A 3-month follow-up study. J Neurol 2010;258:277-83.  Back to cited text no. 7
    
8.
Yri HM, Wegener M, Sander B, Jensen R. Idiopathic intracranial hypertension is not benign: A long-term outcome study. J Neurol 2012;259:886-94.  Back to cited text no. 8
    
9.
Kaufhold F, Kadas EM, Schmidt C, Kunte H, Hoffmann J, Zimmermann H, et al. Optic nerve head quantification in idiopathic intracra-nial hypertension by spectral domain OCT. PLoS One 2012;7:e36965.  Back to cited text no. 9
    
10.
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;53:4069-75.  Back to cited text no. 10
    
11.
Huang-Link YM, Al-Hawasi A, Oberwahrenbrock T. OCT measurements of optic nerve head changes in idiopathic intracranial hypertension. Clin Neurol Neurosurg 2015;130:122-7.  Back to cited text no. 11
    
12.
Rebolleda G, Munoz-Negrete FJ. Follow-up of mild papilledema in idiopathic intracranial hypertension with optical coherence tomography. Invest Ophthalmol Vis Sci 2009;50:5197-200.  Back to cited text no. 12
    
13.
Riva CE, Titze P, Hero M, Petrig BL. Effect of acute decreases of perfusion pressure on choroidal blood flow in humans. Invest Ophthalmol Vis Sci 1997;38:1752-60.  Back to cited text no. 13
    
14.
Cao J, McLeod S, Merges CA, Lutty GA. Choriocapillaris degeneration and related pathologic changes in human diabetic eyes. Arch Ophthalmol 1998;116:589-97.  Back to cited text no. 14
    
15.
Vaghela V, Hingwala DR, Kapilamoorthy TR, Kesavadas C, Thomas B. Spontaneous intracranial hypo and hypertensions: an imaging review. Neurol India 2011;59:506-12.  Back to cited text no. 15
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