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Eye Movements, Strabismus, Amblyopia and Neuro-ophthalmology  |   June 2012
Quantification of Retinal Neural Loss in Patients with Neuromyelitis Optica and Multiple Sclerosis with or without Optic Neuritis Using Fourier-Domain Optical Coherence Tomography
Author Affiliations & Notes
  • Mário L. R. Monteiro
    Division of Ophthalmology and Laboratory of Investigation in Ophthalmology (LIM 33), University of São Paulo Medical School, São Paulo, Brazil; and the
  • Danilo B. Fernandes
    Division of Ophthalmology and Laboratory of Investigation in Ophthalmology (LIM 33), University of São Paulo Medical School, São Paulo, Brazil; and the
  • Samira L. Apóstolos-Pereira
    Department of Neurology, University of São Paulo Medical School, São Paulo, Brazil.
  • Dagoberto Callegaro
    Department of Neurology, University of São Paulo Medical School, São Paulo, Brazil.
  • Corresponding author: Mário Luiz Ribeiro Monteiro, Av. Angélica 1757 conj. 61, 01227-200, São Paulo, S.P., Brazil; [email protected]
Investigative Ophthalmology & Visual Science June 2012, Vol.53, 3959-3966. doi:https://doi.org/10.1167/iovs.11-9324
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      Mário L. R. Monteiro, Danilo B. Fernandes, Samira L. Apóstolos-Pereira, Dagoberto Callegaro; Quantification of Retinal Neural Loss in Patients with Neuromyelitis Optica and Multiple Sclerosis with or without Optic Neuritis Using Fourier-Domain Optical Coherence Tomography. Invest. Ophthalmol. Vis. Sci. 2012;53(7):3959-3966. https://doi.org/10.1167/iovs.11-9324.

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      © ARVO (1962-2015); The Authors (2016-present)

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Abstract

Purpose.: We compared retinal nerve fiber layer (RNFL) and macular thickness measurements in patients with multiple sclerosis (MS) and neuromyelitis optica (NMO) with or without a history of optic neuritis, and in controls using Fourier-domain (FD) optical coherence tomography (OCT).

Methods.: Patients with MS (n = 60), NMO (n = 33), longitudinal extensive transverse myelitis (LETM, n = 28) and healthy controls (n = 41) underwent ophthalmic examination, including automated perimetry, and FD-OCT RNFL and macular thickness measurements. Five groups of eyes were compared: MS with or without previous optic neuritis, NMO, LETM, and controls. Correlation between OCT and visual field (VF) findings was investigated.

Results.: With regard to most parameters, RNFL and macular thickness measurements were significantly smaller in eyes of each group of patients compared to controls. MS eyes with optic neuritis did not differ significantly from MS eyes without optic neuritis, but measurements were smaller in NMO eyes than in all other groups. RNFL (but not macular thickness) measurements were significantly smaller in LETM eyes than in controls. While OCT abnormalities were correlated significantly with VF loss in NMO/LETM and MS, the correlation was much stronger in the former.

Conclusions.: Although FD-OCT RNFL and macular thickness measurements can reveal subclinical or optic neuritis-related abnormalities in NMO-spectrum and MS patients, abnormalities are predominant in the macula of MS patients and in RFNL measurements in NMO patients. The correlation between OCT and VF abnormalities was stronger in NMO than in MS, suggesting the two conditions differ regarding structural and functional damage. (ClinicalTrials.gov number, NCT01024985.)

Introduction
Over the last years, several studies have suggested that retinal nerve fiber layer (RNFL) and macular thickness analysis using optical coherence tomography (OCT) may be used to detect axonal loss in multiple sclerosis (MS) and monitor treatment efficacy. 15 It also has been suggested that OCT abnormalities can help differentiate MS from neuromyelitis optica (NMO) based on the severity of axonal loss and the presence of subclinical damage (reportedly absent in NMO). 3,6 Despite the large number of studies, several issues remain open to question. While there is clear evidence that significant axonal loss is correlated with visual dysfunction in eyes with optic neuritis (ON) from MS, 2,7 few studies have evaluated the relationship between axonal and visual field (VF) loss. 8 Furthermore, while previous studies confirm the occurrence of subclinical retinal axonal damage in MS, 9,10 such damage in patients with longitudinally extensive transverse myelitis (LETM) without ON (considered NMO spectrum patients) is not well established. 3,6 Finally, most studies have been based on average RNFL and macular thickness measurements, while studies evaluating focal neural loss and its correlation with VF findings still are lacking. 
Most OCT studies on demyelinating diseases have used time-domain (TD) technology. 16,8 A more recent development, 3-dimensional (3D) OCT, uses Fourier-domain (FD) detection to provide increased resolution in relation to TD-OCT. However, few studies using FD-OCT have evaluated MS patients 1114 and, to our knowledge, none as yet has assessed patients with NMO. Therefore, the purpose of our study was to evaluate RNFL and macular thickness measurements using FD-OCT in patients with MS with or without a history of ON, and in patients with NMO (affected with ON) or LETM (NMO-spectrum without ON). To our knowledge, this is the first study to evaluate MS and NMO/LETM patients using FD-OCT. We found that axonal loss is predominant in the macula of MS patients and in the RFNL of NMO patients. We also investigated in detail the correlation between FD-OCT RNFL and macular thickness measurements with VF assessment using standard automated perimetry (SAP) and found it to be stronger in NMO than in MS patients. 
Materials and Methods
Study Design and Sampling
This observational, prospective cross-sectional study was approved by our Institutional Review Board Ethics Committee, which followed the principles of the Declaration of Helsinki with informed consent obtained from participants. 
We evaluated 60 patients with MS, 33 with NMO, 28 with LETM and 42 controls. MS and NMO were diagnosed based on current diagnostic criteria. 15,16 NMO patients had a history of ON and acute transverse myelitis. Of the patients 17 (52%) were positive for anti-aquaporine-4 antibodies. LETM patients were included because it has been considered to be a component of the NMO spectrum 17 ; therefore, these patients are considered equivalent to those with NMO without ON. Inclusion criteria for the LETM patients were monophasic or recurrent bilateral neurologic dysfunction attributable to the spinal cord, and progression to nadir between 4 hours and 21 days; inflammation within the spinal cord demonstrated by cerebrospinal fluid or MRI analysis; and spinal cord MRI abnormality extending three or more vertebral segments. A total of 11 (41%) patients had positive anti-aquaporine-4 antibodies. 
The neurologic exclusion criteria for all patients were central nervous system manifestation of infectious diseases and brain MRI abnormalities other than those of MS or NMO. 
History of ON episodes was determined by self-report and physician report, and confirmed by medical record review. Patients whose most recent attack of ON had occurred less than 6 months previously were not included. Controls consisted of normal healthy hospital staff volunteers. 
OCT
Subjects underwent FD-OCT scanning without pupillary dilation, using commercially available equipment (3D OCT-1000; Topcon Corp., Tokyo, Japan) on the same day as the ophthalmic evaluation. The scanning protocol involved the acquisition of a set of 3 OCT images of the optic nerve head (ONH) and macula in a raster pattern covering a 6-mm area with a scan density of 512 × 128 pixels in ∼ 3.5 seconds (27,000 A scans/sec, Figs. 1A, 1B). Criteria for acceptable images included no large eye movements, defined as an abrupt shift completely disconnecting a large retinal vessel; consistent signal intensity level across the scan, and no black bands (caused by blinking) throughout the examination. 
Figure 1. 
 
Top row: demarcation of areas in the macula (A) and optic nerve (B) scanned by Fourier-Domain optical coherence tomography. Middle row: schematic representation of a macular thickness map (C) and retinal nerve fiber layer thickness (D) of a normal individual. Bottom row: demarcation of points read on 24–2 standard automated perimetry (E). The 12 points contained in the central circle correspond to the area evaluated in the circular macular map. (F) Division of the 24 visual field test points and the optic nerve head into sectors, derived from a published optic disc visual field map. 18
Figure 1. 
 
Top row: demarcation of areas in the macula (A) and optic nerve (B) scanned by Fourier-Domain optical coherence tomography. Middle row: schematic representation of a macular thickness map (C) and retinal nerve fiber layer thickness (D) of a normal individual. Bottom row: demarcation of points read on 24–2 standard automated perimetry (E). The 12 points contained in the central circle correspond to the area evaluated in the circular macular map. (F) Division of the 24 visual field test points and the optic nerve head into sectors, derived from a published optic disc visual field map. 18
OCT parameters were calculated automatically by the equipment's software. RNFL thickness measurements were taken using a circular (Ø = 3.4 mm) peripapillary map, when taking measurements corresponding to overall average thickness (360° measure), and the following ONH sectors: temporal (310°–41°), superotemporal (41°–80°), superonasal (80°–120°), nasal (121°–230°), inferonasal (231°–270°), and inferotemporal (271°–310°). The macular thickness measurements were measured on the Early Treatment Diabetic Retinopathy Study (ETDRS) map. The parameters registered were superior outer, inferior outer, temporal outer, nasal outer, superior inner, inferior inner, temporal inner, nasal inner, and average macular thickness. Average macular thickness corresponded to the weighted average of the sectoral macular thickness measurements excluding the fovea (Figs. 1C, 1D). 
Visual Function Testing
Subjects underwent a complete ophthalmologic examination, including best-corrected visual acuity assessment and SAP with the 24-2 SITA-Standard strategy (Humphrey Field Analyzer; Carl-Zeiss Meditec, Dublin, CA) using Goldmann size III stimulus. 
The severity of VF defects was evaluated based on the total deviation plot provided by the equipment. Deviation from normal at each test location was measured in decibels. Unlogged 1/Lambert values were calculated by dividing the decibel readings by 10 and then unlogging the quotient. Values were averaged to calculate the mean deviation (MD) in 1/Lambert units. We also calculated VF sensitivity loss from the 12 central points of the VF, an area roughly equivalent to that covered by OCT scanning in the macular area (Fig. 1E). The 12 values, were averaged to calculate the central mean deviation (CMD). Sensitivity loss also was determined for six VF sectors according to a previously published map, 18 corresponding to the inferonasal, inferotemporal, temporal, superotemporal, superonasal, and nasal ONH sector (Fig. 1F). 
Ophthalmologic inclusion criteria were best-corrected visual acuity ≥20/200 in at least one eye for patients and 20/20 for controls, spherical refraction within ± 5 diopters (D) and cylinder refraction within ± 4 D, intraocular pressure <22 mm Hg, and reliable VF. Exclusion criteria were history of optic neuropathies other than ON, history or clinical signs of glaucoma, and optic disc anomaly. 
Data Analysis and Statistics
OCT measurements parameters of different groups were compared using generalized estimating equation (GEE) models to account for intereye dependencies. Receiver operating characteristic (ROC) curves were used to describe the ability of OCT parameters to discriminate eyes in different groups of individuals from controls. Pearson's correlation coefficients were used to assess possible associations between OCT and VF parameters. Statistical significance was defined as P < 0.05. 
Results
A total of 306 eyes was evaluated; 119 from 60 MS patients, 51 from 33 NMO patients, 54 from 28 patients with LETM, and 82 from 41 controls. Table 1 shows the subjects' demographic data. There was no significant difference between age or sex in the groups studied. MS and NMO eyes had MD significantly worse than that of controls and patients with LETM. 
Table 1. 
 
Demographic Characteristics of Patients with MS, NMO, and LETM, and Disease-Free Controls
Table 1. 
 
Demographic Characteristics of Patients with MS, NMO, and LETM, and Disease-Free Controls
MS NMO LETM Controls
Subjects 60 33 28 41
Eyes studied 119 51 54 82
Eyes affected by ON (%) 45 (38.3) 62 (93.9)
Mean age ± SD (y) 35.6 ± 9.4 39.9 ± 11.6 40.1 ± 10.3 36.6 ± 12.3
Sex n (% female) 50 (83.3) 30 (90.9) 18 (64.3) 35 (85.4)
Median visual acuity (range) 20/20 (20/16–20/200) 20/25 (20/16–20/200) 20/20 (20/16–20/25) 20/20 (20/16−20/20)
Mean visual field MD ± SD (dB) −3.56 ± 4.4 −10.82 ± 8.73 −1.38 ± 1.18 −1.16 ± 1.06
The eyes were organized into 5 groups: MS with ON (MS + ON, n = 45), MS without ON (MS − ON, n = 74), NMO with ON (NMO + ON, n = 51), LETM (n = 54), and controls (n = 82). There were 18 eyes excluded due to poor vision (MS = 1, NMO = 15), retinal vein occlusion (LETM = 1), or macular scarring (LETM = 1). 
Figure 2 depicts examples of FD-OCT RNFL and macular thickness measurements. Figure 3 and Table 2 show RNFL and macular thickness measurements for all groups. The groups differed significantly with regard to each study parameter (P < 0.001, GEE). Regarding RNFL thickness, there was no significant difference between MS + ON and MS − ON, except for the temporal and superotemporal sectors. MS + ON also did not differ significantly from LETM except for the temporal sector. Similarly, MS − ON RNFL measurements did not differ significantly from LETM. On the other hand, NMO + ON measurements for the most part were significantly smaller than MS + ON, MS − ON, and LETM measurements. The groups also differed significantly with regard to each macular thickness study parameter (P < 0.001). MS + ON macular measurements were significantly smaller than MS − ON with regard to the average, superior inner, temporal inner, nasal inner, and nasal outer measurements. MS + ON did not differ significantly from NMO + ON in any parameter. On the other hand MS − ON did not differ significantly from LETM in any parameter except for the temporal outer segment. MS + ON and NMO + ON differed significantly from LETM with regard to all parameters. Finally MS − ON differed significantly from NMO + ON with regard to most parameters. 
Figure 2. 
 
Examples of FD-OCT retinal nerve fiber layer (above) and macular (below) thickness measurements generated by the Topcon 3 D OCT-1000 equipment in eyes of patients with MS, eyes with (A) or without (B) ON, NMO (C), and LETM (D). Measurements in different sectors are indicated with numbers and represented in colors that correspond to the normal distribution. Sectors indicate values within normal range (green), and less than the fifth (yellow), less than the first (red), and greater than the 95th (white) percentiles compared to an age-matched reference population.
Figure 2. 
 
Examples of FD-OCT retinal nerve fiber layer (above) and macular (below) thickness measurements generated by the Topcon 3 D OCT-1000 equipment in eyes of patients with MS, eyes with (A) or without (B) ON, NMO (C), and LETM (D). Measurements in different sectors are indicated with numbers and represented in colors that correspond to the normal distribution. Sectors indicate values within normal range (green), and less than the fifth (yellow), less than the first (red), and greater than the 95th (white) percentiles compared to an age-matched reference population.
Figure 3. 
 
Mean macular and RNFL measurements in eyes of patients with MS with or without ON, NMO, LETM, and controls. (A) average and sectoral macular thickness measurements. (B) average and sectoral RNFL thickness measurements. * P < 0.05 when compared to controls.
Figure 3. 
 
Mean macular and RNFL measurements in eyes of patients with MS with or without ON, NMO, LETM, and controls. (A) average and sectoral macular thickness measurements. (B) average and sectoral RNFL thickness measurements. * P < 0.05 when compared to controls.
Table 2. 
 
Mean (SE) RNFL and Macular Thickness Parameters (in mm) ± SD for Eyes of Patients with MS, NMO, LETM, and Normal Controls
Table 2. 
 
Mean (SE) RNFL and Macular Thickness Parameters (in mm) ± SD for Eyes of Patients with MS, NMO, LETM, and Normal Controls
OCT Parameters MS + ON Eyes (SD) (n = 45) MS − ON Eyes (SD) (n = 74) NMO Eyes (SD) (n = 51) LETM Eyes (n = 53) Control Eyes (n = 82) MS + ON vs. MS − ON P Value MS + ON vs. NMO P Value MS + ON vs. LETM P Value MS − ON vs. NMO P Value MS − ON vs. LETM P Value NMO vs. LETM P Value
RNFL average 94.6 (19.0) 101.2 (11.6) 82.7 (22.4) 97.9 (10.7) 107.6 (9.4) 0.06 0.02 0.41 <0.001 0.12 0.001
RNFL sector
 Superotemporal 117.0 (25.6) 127.6 (16.3) 103.0 (28.0) 123.8 (15.4) 137.2 (15.2) 0.04 0.03 0.21 <0.001 0.23 <0.001
 Superonasal 105.8 (23.7) 107.6 (18.8) 97.0 (28.1) 107.0 (18.0) 117.9 (18.0) 0.58 0.18 0.82 0.03 0.67 0.07
 Nasal 88.4 (17.4) 93.3 (13.2) 75.4 (21.0) 87.1 (16.3) 96.7 (15.2) 0.14 0.006 0.75 <0.001 0.053 0.010
 Inferonasal 113.5 (31.1) 117.9 (19.5) 93.6 (31.1) 113.5 (20.7) 125.7 (17.9) 0.38 0.008 0.99 <0.001 0.25 0.002
 Inferotemporal 120.3 (30.0) 131.4 (26.3) 103.5 (35.9) 129.3 (18.4) 141.9 (17.9) 0.39 0.04 0.14 <0.001 0.35 <0.001
 Temporal 67.2 (17.4) 75.4 (12.3) 62.7 (21.3) 74.8 (10.8) 79.4 (11.5) 0.02 0.36 0.04 0.001 0.67 0.003
Macular average 255.2 (17.3) 262.4 (16.4) 253.2 (16.6) 269.2 (13.3) 272.7 (13.2) 0.04 0.64 <0.001 0.007 0.06 <0.001
Macular sector
 Superior inner 277.8 (18.9) 288.1 (19.6) 272.3 (18.9) 294.2 (15.2) 297.7 (17.8) 0.006 0.21 <0.001 <0.001 0.16 <0.001
 Temporal inner 265.9 (17.4) 273.8 (18.3) 262.3 (17.9) 279.4 (17.1) 283.4 (16.0) 0.03 0.38 0.001 0.001 0.21 <0.001
 Inferior inner 275.6 (19.8) 281.8 (20.1) 270.1 (20.6) 286.1 (18.2) 291.6 (17.8) 0.11 0.26 0.02 0.004 0.39 <0.001
 Nasal inner 276.7 (21.3) 287.8 (18.7) 273.6 (23.1) 293.7 (16.9) 299.9 (16.8) 0.005 0.55 <0.001 0.001 0.19 <0.001
 Superior outer 244.6 (17.7) 250.9 (15.3) 242.7 (17.8) 257.2 (15.3) 258.3 (15.3) 0.07 0.68 0.003 0.02 0.10 0.001
 Temporal outer 230.8 (14.9) 234.7 (17.5) 232.2 (13.9) 243.9 (15.2) 242.4 (13.6) 0.26 0.70 0.001 0.41 0.02 0.001
 Temporal outer 230.8 (14.9) 234.7 (17.5) 232.2 (13.9) 243.9 (15.2) 242.4 (13.6) 0.26 0.70 0.001 0.41 0.02 0.001
 Nasal outer 253.7 (22.1) 263.7 (18.1) 252.8 (23.3) 272.2 (15.9) 277.8 (14.9) 0.02 0.88 <0.001 0.01 0.05 <0.001
Table 3 shows comparisons between patients and controls corresponding to RNFL and macular thickness measurements. MS + ON RNFL thickness measurements differed significantly from controls in all parameters. MS − ON differed significantly from controls in all parameters except for the nasal and temporal sectors. NMO eyes differed significantly from controls in all parameters. LETM eyes, although not affected by ON, also differed significantly from controls with regard to all parameters studied. With regard to macular thickness measurements, MS + ON, MS − ON, and NMO + ON differed significantly from controls in all parameters, while LETM did not differ significantly from controls in any parameter (Table 3). 
Table 3. 
 
Comparison between Controls and Eyes of Patients with MS, with MS + ON, or without Opti, NMO, or LETM with AROC
Table 3. 
 
Comparison between Controls and Eyes of Patients with MS, with MS + ON, or without Opti, NMO, or LETM with AROC
MS + ON vs. Controls MS − ON vs. Controls NMO vs. Controls LETM vs. Controls
P Values AROC (SE) P Values AROC (SE) P Values AROC (SE) P Values AROC (SE)
RNFL parameter
 Average <0.001 0.69 (0.05) <0.001 0.68 (0.04) <0.001 0.84 (0.04) <0.001 0.75 (0.04)
 Superotemporal sector <0.001 0.75 (0.05) <0.001 0.67 (0.04) <0.001 0.85 (0.04) <0.001 0.74 (0.04)
 Superonasal sector 0.007 0.65 (0.05) 0.001 0.65 (0.04) <0.001 0.72 (0.05) 0.001 0.67 (0.05)
 Nasal sector 0.02 0.63 (0.05) 0.19 0.56 (0.05) <0.001 0.79 (0.04) 0.003 0.65 (0.05)
 Inferonasal sector 0.03 0.62 (0.06) 0.008 0.62 (0.05) <0.001 0.80 (0.04) 0.006 0.71 (0.05)
 Inferotemporal sector <0.001 0.71 (0.05) 0.008 0.62 (0.05) <0.001 0.82 (0.04) 0.001 0.69 (0.05)
 Temporal sector <0.001 0.71 (0.05) 0.08 0.58 (0.05) <0.001 0.79 (0.05) 0.08 0.59 (0.05)
Macular parameter
 Average <0.001 0.81 (0.05) <0.001 0.68 (0.04) <0.001 0.82 (0.04) 0.15 0.57 (0.05)
 Superior inner <0.001 0.77 (0.05) 0.007 0.63 (0.05) <0.001 0.83 (0.04) 0.29 0.55 (0.05)
 Temporal inner <0.001 0.78 (0.05) 0.002 0.64 (0.04) <0.001 0.80 (0.04) 0.18 0.57 (0.05)
 Inferior inner <0.001 0.74 (0.05) 0.006 0.63 (0.05) <0.001 0.78 (0.04) 0.14 0.57 (0.05)
 Nasal inner <0.001 0.80 (0.04) 0.001 0.65 (0.04) <0.0001 0.81 (0.04) 0.12 0.58 (0.05)
 Superior outer <0.001 0.74 (0.05) 0.005 0.63 (0.05) <0.001 0.74 (0.05) 0.43 0.54 (0.05)
 Temporal outer <0.001 0.72 (0.05) 0.001 0.65 (0.04) 0.001 0.68 (0.05) 0.62 0.52 (0.05)
 Inferior outer <0.001 0.76 (0.05) <0.001 0.68 (0.04) <0.001 0.72 (0.05) 0.20 0.57 (0.05)
 Nasal outer <0.001 0.82 (0.05) <0.001 0.71 (0.04) <0.001 0.80 (0.04) 0.11 0.61 (0.05)
Table 3 also shows the area under the ROC curve (AROC) values corresponding to RNFL and macular thickness measurements comparisons of each group and controls. While both sets of measurements were able to discriminate MS + ON eyes from controls, the discrimination ability was greater significantly for macular thickness (AROC range 0.72–0.80) than for RNFL thickness parameters (AROC range 0.63–0.74). The same was true for MS − ON (0.63–0.71 vs. 0.57–0.68, respectively), but not for NMO + ON (0.68–0.81 vs. 0.73–0.84, respectively). Finally, while LETM differed significantly from controls with regard to most RNFL thickness parameters (AROC range 0.59–0.75), no significant difference was observed for macular thickness measurements (AROC range 0.52–0.65). 
Table 4 shows the correlation between macular and RNFL thickness measurements with VF sensitivity loss assessed globally (MD), in 12 central test points (CMD) and in six VF areas. Correlations between OCT and VF findings were significantly greater for patients in the NMO spectrum (range 0.26–0.57) than for MS patients (range 0.10–0.36). The difference was even more striking for macular thickness measurements: correlations ranged from 0.36–0.52 in NMO patients and from 0.06–0.25 (frequently non-significant) in MS patients. In NMO patients, the three most significant correlations (P < 0.001) were between RNFL thickness in the superotemporal sector and VF sector 4 (r = 0.57) or the MD (r = 0.55), and average RNFL thickness and VF sector 4 (r = 0.53). In MS patients, the three most significant correlations were between VF sector 6 and average or temporal RNFL thickness (r = 0.36), and between VF sector 6 and inferotemporal RNFL thickness (r = 0.35). 
Table 4. 
 
Relationship between 3D OCT-1000 Macular and RNFL Thickness Parameters, and Visual Field Sensitivity Parameters in Different Field Sectors
Table 4. 
 
Relationship between 3D OCT-1000 Macular and RNFL Thickness Parameters, and Visual Field Sensitivity Parameters in Different Field Sectors
OCT Parameter Visual Field Parameter (1/Lambert)
MD CMD Visual Field Sector
1 2 3 4 5 6
MS NMO MS NMO MS NMO MS NMO MS NMO MS NMO MS NMO MS NMO
Average thickness
 Macular 0.15 0.52* 0.21† 0.36* 0.18 0.40* 0.06 0.41* 0.04 0.40* 0.20† 0.43* 0.19 0.39* 0.25† 0.35*
 RNFL 0.29‡ 0.43* 0.34* 0.48* 0.25† 0.45* 0.20† 0.44* 0.18 0.48* 0.31* 0.53* 0.33* 0.49* 0.36* 0.45*
Sectoral RNFL thickness
 Nasal 0.28‡ 0.40* 0.31‡ 0.32* 0.21† 0.38* 0.20† 0.33* 0.18 0.37* 0.30‡ 0.39* 0.33* 0.42* 0.33* 0.31‡
 Superonasal 0.15 0.36* 0.13 0.33* 0.13 0.37* 0.14 0.26† 0.10 0.31‡ 0.15 0.39* 0.19 0.33* 0.11 0.32*
 Superotemporal 0.26† 0.55* 0.29‡ 0.52* 0.28 0.46* 0.15 0.47* 0.14 0.50* 0.30‡ 0.57* 0.30‡ 0.52* 0.32* 0.49*
 Temporal 0.26† 0.38* 0.32* 0.38* 0.21† 0.32* 0.17 0.33* 0.17 0.36* 0.28‡ 0.40* 0.26‡ 0.34* 0.36* 0.36*
 Inferotemporal 0.25† 0.52* 0.32* 0.49* 0.24† 0.37* 0.17 0.34* 0.13 0.51* 0.30‡ 0.51* 0.25† 0.45* 0.35* 0.46*
 Inferonasal 0.17 0.42* 0.23† 0.40* 0.14 0.33* 0.11 0.34* 0.10 0.41* 0.19 0.43* 0.21† 0.38* 0.22† 0.37*
Discussion
We evaluated a large population of patients in the NMO spectrum, and compared FD-OCT findings of NMO and MS patients with and without a history of ON. Our data confirmed the ability of OCT to quantify axonal loss in these conditions. In MS + ON, a significant loss of RNFL compared to normals was observed with regard to overall average and all RNFL sectors except for the nasal, in agreement with previous studies reporting reduced average 1,2,1922 and sectoral 2,5,20,23,24 RNFL thickness measurements in MS eyes with ON. We also found subclinical RFNL loss in MS eyes without ON history in accordance with previous studies using TD-OCT. 2,3,5,9,19,21,22,24,25  
Our study also confirmed that MS patients have significantly reduced macular thickness measurements. 3,5,11,26 Interestingly, however, OCT abnormalities in MS patients were much more pronounced in macular than RNFL thickness measurements (Fig. 3 and Table 2). The ROC curve analysis also indicates greater discrimination ability for macular thickness than for RNFL thickness measurements in MS patients (Table 3). Since studies evaluating OCT measurements indicate that macular thickness measurements are not more efficient than RNFL thickness measurements at detecting neural loss in different optic neuropathies, 27,28 we believe the greater discrimination ability observed for MS patients in our study is an indication that macular thickness measurements reflect the reduction not only of RGC, but also of other retinal layers. This interpretation is in accordance with recent data indicating that MS patients can present primary damage to retinal layers irrespective of RGCs, including the inner nuclear layer atrophy. 11,29  
Our findings provide new information regarding the use of FD-OCT measurements in eyes of patients in the NMO spectrum. They also confirm the occurrence of greater loss of RNFL thickness in NMO than in MS patients (Fig. 3, Table 2), as observed in previous studies using TD-OCT technology. 3,6,3033 These findings are supported by clinical findings of greater reduction in visual acuity and VF in NMO. 34 On the other hand, the results of our macular thickness measurements provided important new information. To our knowledge, only Ratchford et al. evaluated macular thickness measurements in NMO patients, and found a significant difference in average measurements compared to normals and MS patients. 3 In our study, however, while a significant reduction in all macular measurements was found when compared to normals, the comparison between NMO and MS patients yielded somewhat unexpected findings: while RNFL thickness measurements were significantly lower in NMO than in MS + ON, the two groups did not differ with regard to macular thickness measurements (Table 2). We believe this finding is a further indication that in MS patients macular thickness reduction is the result of damage to retinal layers other than the RGC layer, as observed in previous histopathologic and OCT studies. 11,29  
Our study also is important in that we compared MS and NMO patients by analyzing eyes without a history of ON. To do so, we evaluated 54 eyes of 28 patients with LETM (considered part of the NMO spectrum). Our data indicated that, like eyes affected with MS, eyes in the NMO spectrum also presented subclinical reduction of the RNFL. This finding differs from previous studies claiming that subclinical axonal loss occurs in MS but not in patients in the NMO spectrum—a fact that presumably would make it possible to differentiate the two conditions. Thus, while subclinical axonal loss on OCT in eyes of patients with MS without a history of ON is well documented, the possibility of subclinical axonal loss in eyes in the NMO spectrum is not acknowledged generally. Two previous studies found no retinal axonal loss in eyes with LETM, but only a small number of patients were investigated. Ratchford et al. found no significant reduction in the RNFL thickness of non-affected eyes of patients with NMO or LETM. 3 They suggested that OCT could help differentiate non-affected eyes of LETM or NMO patients from eyes of patients with MS, but only average RNFL thickness measurements were compared and the sample of NMO or LETM patients with non-affected eyes was small (8 and 17, respectively). Likewise, de Seze et al. found no subclinical RNFL loss in a sample of 8 non-affected eyes of patients with LETM and positive anti-NMO antibodies. 30 However, in a previous study of 17 LETM patients using TD-OCT, we found subclinical abnormalities in one quadrant and in one 30-degree segment of the disc. 35 In the present study, using a larger sample (28 patients, 54 eyes) and FD-OCT equipment, we found a significant reduction in RNFL thickness measurements in several parameters (Table 2). Therefore, the presence of subclinical retinal axonal loss should not be used in the differential diagnosis of eyes with MS and eyes in the NMO spectrum. 
Our current study also investigated the relationship between FD-OCT and SAP in MS and NMO patients using global and sectoral measurements. While several investigators have found a strong correlation between OCT measurements and visual acuity, contrast sensitivity, or frequency doubling perimetry, 2,5,7,10,14,22,31,36,37 few have investigated the relationship between OCT and SAP. In a sample of MS patients, Henderson et al. found a significant correlation between VF mean deviation in dB and average RNFL thickness or macular volume (r = 0.31, P = 0.038, and r = 0.34, P = 0.022, respectively). 5 Four other studies found correlation coefficients between average RNFL (but not macular) OCT measurements and global MD VF loss in MS patients ranging from 0.22 and 0.51. 7,24,25,36 Cheng et al. evaluated the relationship between average or quadrantic RFNL thickness loss and global or sectoral VF loss, and found a strong association between OCT measures and VF in all sectoral measurements evaluated, particularly between the inferior optic disc quadrant and the corresponding VF loss in the superotemporal area (r = −0.65). 8 Macular thickness measurements were not investigated. Only one study evaluated the correlation between OCT measurements and VF loss in NMO patients, and reported a significant correlation (r = −0.78), but provided no details on how the correlation was assessed. 30  
In our study, significant differences in structure-function relationships were observed between MS and NMO, mainly in macular thickness measurements. Thus, when evaluating the relationship between RNFL thickness and VF loss, the correlation coefficients were slightly greater for eyes in the NMO spectrum (from 0.36–0.57, depending on the sector) than for MS eyes (from 0.10–0.36), matching the results of several studies in MS patients, 5,7,8,24,25,36 and one in NMO patients. 30 However, the difference between the two diseases was striking when investigating the correlation between VF and macular thickness measurements. The corresponding correlation coefficients were 0.36–0.52 for eyes in the NMO spectrum and 0.06–0.25 (frequently non-significant) for MS eyes. We believe the discrepancy may be ascribed to differences in retinal pathology between the two conditions. The presumption that reduced macular thickness in NMO patients is the direct result of RGC atrophy from axonal damage in the optic nerve would explain the similarities in correlation coefficients of the two types of measurements. In relapsing-remitting MS patients, however, recent studies indicate that macular thickness measurements are influenced by structures other than the RGCs. 11,29 Future studies using segmental analysis of FD-OCT macular thickness measurements and larger samples are necessary to confirm this finding. 
In conclusion, our study shows that, while OCT-measured axonal loss usually is more severe in NMO patients, subclinical neuronal loss can occur in both diseases and, therefore, should not be considered in differential diagnosis. Axonal loss appears to be equally detectable in RNFL and macular measurements in NMO patients, but more evident in macular thickness measurements in MS patients. Accordingly, the two conditions differed significantly regarding the relationship between retinal axonal loss and VF deficit. Clinicians should take these differences into account when using OCT measurements for diagnosis and follow-up of MS or NMO patients. 
Acknowledgments
Donald Hood provided editorial review of the manuscript. 
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Footnotes
 Supported by grants from Fundação de Amparo a Pesquisa do Estado de São Paulo FAPESP (2009/50174-0), São Paulo, Brazil, and from Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq (306487/2011-0), Brasília, Brazil.
Footnotes
 Disclosure: M.L.R. Monteiro, None; D.B. Fernandes, None; S.L. Apóstolos-Pereira, None; D. Callegaro, None
Figure 1. 
 
Top row: demarcation of areas in the macula (A) and optic nerve (B) scanned by Fourier-Domain optical coherence tomography. Middle row: schematic representation of a macular thickness map (C) and retinal nerve fiber layer thickness (D) of a normal individual. Bottom row: demarcation of points read on 24–2 standard automated perimetry (E). The 12 points contained in the central circle correspond to the area evaluated in the circular macular map. (F) Division of the 24 visual field test points and the optic nerve head into sectors, derived from a published optic disc visual field map. 18
Figure 1. 
 
Top row: demarcation of areas in the macula (A) and optic nerve (B) scanned by Fourier-Domain optical coherence tomography. Middle row: schematic representation of a macular thickness map (C) and retinal nerve fiber layer thickness (D) of a normal individual. Bottom row: demarcation of points read on 24–2 standard automated perimetry (E). The 12 points contained in the central circle correspond to the area evaluated in the circular macular map. (F) Division of the 24 visual field test points and the optic nerve head into sectors, derived from a published optic disc visual field map. 18
Figure 2. 
 
Examples of FD-OCT retinal nerve fiber layer (above) and macular (below) thickness measurements generated by the Topcon 3 D OCT-1000 equipment in eyes of patients with MS, eyes with (A) or without (B) ON, NMO (C), and LETM (D). Measurements in different sectors are indicated with numbers and represented in colors that correspond to the normal distribution. Sectors indicate values within normal range (green), and less than the fifth (yellow), less than the first (red), and greater than the 95th (white) percentiles compared to an age-matched reference population.
Figure 2. 
 
Examples of FD-OCT retinal nerve fiber layer (above) and macular (below) thickness measurements generated by the Topcon 3 D OCT-1000 equipment in eyes of patients with MS, eyes with (A) or without (B) ON, NMO (C), and LETM (D). Measurements in different sectors are indicated with numbers and represented in colors that correspond to the normal distribution. Sectors indicate values within normal range (green), and less than the fifth (yellow), less than the first (red), and greater than the 95th (white) percentiles compared to an age-matched reference population.
Figure 3. 
 
Mean macular and RNFL measurements in eyes of patients with MS with or without ON, NMO, LETM, and controls. (A) average and sectoral macular thickness measurements. (B) average and sectoral RNFL thickness measurements. * P < 0.05 when compared to controls.
Figure 3. 
 
Mean macular and RNFL measurements in eyes of patients with MS with or without ON, NMO, LETM, and controls. (A) average and sectoral macular thickness measurements. (B) average and sectoral RNFL thickness measurements. * P < 0.05 when compared to controls.
Table 1. 
 
Demographic Characteristics of Patients with MS, NMO, and LETM, and Disease-Free Controls
Table 1. 
 
Demographic Characteristics of Patients with MS, NMO, and LETM, and Disease-Free Controls
MS NMO LETM Controls
Subjects 60 33 28 41
Eyes studied 119 51 54 82
Eyes affected by ON (%) 45 (38.3) 62 (93.9)
Mean age ± SD (y) 35.6 ± 9.4 39.9 ± 11.6 40.1 ± 10.3 36.6 ± 12.3
Sex n (% female) 50 (83.3) 30 (90.9) 18 (64.3) 35 (85.4)
Median visual acuity (range) 20/20 (20/16–20/200) 20/25 (20/16–20/200) 20/20 (20/16–20/25) 20/20 (20/16−20/20)
Mean visual field MD ± SD (dB) −3.56 ± 4.4 −10.82 ± 8.73 −1.38 ± 1.18 −1.16 ± 1.06
Table 2. 
 
Mean (SE) RNFL and Macular Thickness Parameters (in mm) ± SD for Eyes of Patients with MS, NMO, LETM, and Normal Controls
Table 2. 
 
Mean (SE) RNFL and Macular Thickness Parameters (in mm) ± SD for Eyes of Patients with MS, NMO, LETM, and Normal Controls
OCT Parameters MS + ON Eyes (SD) (n = 45) MS − ON Eyes (SD) (n = 74) NMO Eyes (SD) (n = 51) LETM Eyes (n = 53) Control Eyes (n = 82) MS + ON vs. MS − ON P Value MS + ON vs. NMO P Value MS + ON vs. LETM P Value MS − ON vs. NMO P Value MS − ON vs. LETM P Value NMO vs. LETM P Value
RNFL average 94.6 (19.0) 101.2 (11.6) 82.7 (22.4) 97.9 (10.7) 107.6 (9.4) 0.06 0.02 0.41 <0.001 0.12 0.001
RNFL sector
 Superotemporal 117.0 (25.6) 127.6 (16.3) 103.0 (28.0) 123.8 (15.4) 137.2 (15.2) 0.04 0.03 0.21 <0.001 0.23 <0.001
 Superonasal 105.8 (23.7) 107.6 (18.8) 97.0 (28.1) 107.0 (18.0) 117.9 (18.0) 0.58 0.18 0.82 0.03 0.67 0.07
 Nasal 88.4 (17.4) 93.3 (13.2) 75.4 (21.0) 87.1 (16.3) 96.7 (15.2) 0.14 0.006 0.75 <0.001 0.053 0.010
 Inferonasal 113.5 (31.1) 117.9 (19.5) 93.6 (31.1) 113.5 (20.7) 125.7 (17.9) 0.38 0.008 0.99 <0.001 0.25 0.002
 Inferotemporal 120.3 (30.0) 131.4 (26.3) 103.5 (35.9) 129.3 (18.4) 141.9 (17.9) 0.39 0.04 0.14 <0.001 0.35 <0.001
 Temporal 67.2 (17.4) 75.4 (12.3) 62.7 (21.3) 74.8 (10.8) 79.4 (11.5) 0.02 0.36 0.04 0.001 0.67 0.003
Macular average 255.2 (17.3) 262.4 (16.4) 253.2 (16.6) 269.2 (13.3) 272.7 (13.2) 0.04 0.64 <0.001 0.007 0.06 <0.001
Macular sector
 Superior inner 277.8 (18.9) 288.1 (19.6) 272.3 (18.9) 294.2 (15.2) 297.7 (17.8) 0.006 0.21 <0.001 <0.001 0.16 <0.001
 Temporal inner 265.9 (17.4) 273.8 (18.3) 262.3 (17.9) 279.4 (17.1) 283.4 (16.0) 0.03 0.38 0.001 0.001 0.21 <0.001
 Inferior inner 275.6 (19.8) 281.8 (20.1) 270.1 (20.6) 286.1 (18.2) 291.6 (17.8) 0.11 0.26 0.02 0.004 0.39 <0.001
 Nasal inner 276.7 (21.3) 287.8 (18.7) 273.6 (23.1) 293.7 (16.9) 299.9 (16.8) 0.005 0.55 <0.001 0.001 0.19 <0.001
 Superior outer 244.6 (17.7) 250.9 (15.3) 242.7 (17.8) 257.2 (15.3) 258.3 (15.3) 0.07 0.68 0.003 0.02 0.10 0.001
 Temporal outer 230.8 (14.9) 234.7 (17.5) 232.2 (13.9) 243.9 (15.2) 242.4 (13.6) 0.26 0.70 0.001 0.41 0.02 0.001
 Temporal outer 230.8 (14.9) 234.7 (17.5) 232.2 (13.9) 243.9 (15.2) 242.4 (13.6) 0.26 0.70 0.001 0.41 0.02 0.001
 Nasal outer 253.7 (22.1) 263.7 (18.1) 252.8 (23.3) 272.2 (15.9) 277.8 (14.9) 0.02 0.88 <0.001 0.01 0.05 <0.001
Table 3. 
 
Comparison between Controls and Eyes of Patients with MS, with MS + ON, or without Opti, NMO, or LETM with AROC
Table 3. 
 
Comparison between Controls and Eyes of Patients with MS, with MS + ON, or without Opti, NMO, or LETM with AROC
MS + ON vs. Controls MS − ON vs. Controls NMO vs. Controls LETM vs. Controls
P Values AROC (SE) P Values AROC (SE) P Values AROC (SE) P Values AROC (SE)
RNFL parameter
 Average <0.001 0.69 (0.05) <0.001 0.68 (0.04) <0.001 0.84 (0.04) <0.001 0.75 (0.04)
 Superotemporal sector <0.001 0.75 (0.05) <0.001 0.67 (0.04) <0.001 0.85 (0.04) <0.001 0.74 (0.04)
 Superonasal sector 0.007 0.65 (0.05) 0.001 0.65 (0.04) <0.001 0.72 (0.05) 0.001 0.67 (0.05)
 Nasal sector 0.02 0.63 (0.05) 0.19 0.56 (0.05) <0.001 0.79 (0.04) 0.003 0.65 (0.05)
 Inferonasal sector 0.03 0.62 (0.06) 0.008 0.62 (0.05) <0.001 0.80 (0.04) 0.006 0.71 (0.05)
 Inferotemporal sector <0.001 0.71 (0.05) 0.008 0.62 (0.05) <0.001 0.82 (0.04) 0.001 0.69 (0.05)
 Temporal sector <0.001 0.71 (0.05) 0.08 0.58 (0.05) <0.001 0.79 (0.05) 0.08 0.59 (0.05)
Macular parameter
 Average <0.001 0.81 (0.05) <0.001 0.68 (0.04) <0.001 0.82 (0.04) 0.15 0.57 (0.05)
 Superior inner <0.001 0.77 (0.05) 0.007 0.63 (0.05) <0.001 0.83 (0.04) 0.29 0.55 (0.05)
 Temporal inner <0.001 0.78 (0.05) 0.002 0.64 (0.04) <0.001 0.80 (0.04) 0.18 0.57 (0.05)
 Inferior inner <0.001 0.74 (0.05) 0.006 0.63 (0.05) <0.001 0.78 (0.04) 0.14 0.57 (0.05)
 Nasal inner <0.001 0.80 (0.04) 0.001 0.65 (0.04) <0.0001 0.81 (0.04) 0.12 0.58 (0.05)
 Superior outer <0.001 0.74 (0.05) 0.005 0.63 (0.05) <0.001 0.74 (0.05) 0.43 0.54 (0.05)
 Temporal outer <0.001 0.72 (0.05) 0.001 0.65 (0.04) 0.001 0.68 (0.05) 0.62 0.52 (0.05)
 Inferior outer <0.001 0.76 (0.05) <0.001 0.68 (0.04) <0.001 0.72 (0.05) 0.20 0.57 (0.05)
 Nasal outer <0.001 0.82 (0.05) <0.001 0.71 (0.04) <0.001 0.80 (0.04) 0.11 0.61 (0.05)
Table 4. 
 
Relationship between 3D OCT-1000 Macular and RNFL Thickness Parameters, and Visual Field Sensitivity Parameters in Different Field Sectors
Table 4. 
 
Relationship between 3D OCT-1000 Macular and RNFL Thickness Parameters, and Visual Field Sensitivity Parameters in Different Field Sectors
OCT Parameter Visual Field Parameter (1/Lambert)
MD CMD Visual Field Sector
1 2 3 4 5 6
MS NMO MS NMO MS NMO MS NMO MS NMO MS NMO MS NMO MS NMO
Average thickness
 Macular 0.15 0.52* 0.21† 0.36* 0.18 0.40* 0.06 0.41* 0.04 0.40* 0.20† 0.43* 0.19 0.39* 0.25† 0.35*
 RNFL 0.29‡ 0.43* 0.34* 0.48* 0.25† 0.45* 0.20† 0.44* 0.18 0.48* 0.31* 0.53* 0.33* 0.49* 0.36* 0.45*
Sectoral RNFL thickness
 Nasal 0.28‡ 0.40* 0.31‡ 0.32* 0.21† 0.38* 0.20† 0.33* 0.18 0.37* 0.30‡ 0.39* 0.33* 0.42* 0.33* 0.31‡
 Superonasal 0.15 0.36* 0.13 0.33* 0.13 0.37* 0.14 0.26† 0.10 0.31‡ 0.15 0.39* 0.19 0.33* 0.11 0.32*
 Superotemporal 0.26† 0.55* 0.29‡ 0.52* 0.28 0.46* 0.15 0.47* 0.14 0.50* 0.30‡ 0.57* 0.30‡ 0.52* 0.32* 0.49*
 Temporal 0.26† 0.38* 0.32* 0.38* 0.21† 0.32* 0.17 0.33* 0.17 0.36* 0.28‡ 0.40* 0.26‡ 0.34* 0.36* 0.36*
 Inferotemporal 0.25† 0.52* 0.32* 0.49* 0.24† 0.37* 0.17 0.34* 0.13 0.51* 0.30‡ 0.51* 0.25† 0.45* 0.35* 0.46*
 Inferonasal 0.17 0.42* 0.23† 0.40* 0.14 0.33* 0.11 0.34* 0.10 0.41* 0.19 0.43* 0.21† 0.38* 0.22† 0.37*
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