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(Investigative Ophthalmology and Visual Science. 2001;42:1487-1494.)
© 2001 by The Association for Research in Vision and Ophthalmology, Inc.

Correlation of Optic Nerve Head Tomography with Visual Field Sensitivity in Papilledema

Tommaso Salgarello, Benedetto Falsini, Salvatore Tedesco, Maria Elena Galan, Alberto Colotto and Luigi Scullica

From the Institute of Ophthalmology, Catholic University, Rome, Italy.


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
PURPOSE. To quantify the relationship between optic nerve head tomography and perimetric sensitivity in patients with papilledema.

METHODS. Eight patients with variable degrees of recently diagnosed papilledema associated with idiopathic intracranial hypertension (IIH) were evaluated with confocal scanning laser ophthalmoscopy (CSLO) and automated perimetry. Patients were followed up with serial measurements over a period of 5 to 30 months (mean ± SD, 17.1 ± 9), while under medical treatment (acetazolamide). The tomographic parameters, volume above reference (VAR), volume above surface (VAS), effective mean height (EMH), and maximum height in contour (MxHC), were obtained by tomography, either globally or from predefined disc sectors. The perimetric indices, mean deviation (MD) and pattern SD (PSD), were evaluated. The results from patients’ right eyes and the individual intereye differences in both tomographic and perimetric parameters, were statistically evaluated by nonparametric correlational (Spearman) and repeated measures (Wilcoxon) analyses.

RESULTS. At baseline, all tomographic parameters were negatively correlated with MD in global (r = -0.8) and sectorial (r = -0.6) evaluations. The interocular differences in overall tomographic parameters were correlated with corresponding differences in perimetric MD (r = -0.8) and PSD (r = 0.6). During the follow-up period, volumetric disc parameters decreased (P < 0.02), whereas perimetric MD increased (P = 0.02) at comparable times.

CONCLUSIONS. In patients with recently diagnosed papilledema, optic nerve head tomographic abnormalities are quantitatively correlated with visual field sensitivity losses. Therapeutic improvement of volumetric parameters may be paralleled by recovery in perimetric sensitivity. The data support the possible use of both techniques in combination to monitor the amount of papilledema and the effectiveness of treatments designed to reduce intracranial hypertension.


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
During the past few decades several approaches have been used to analyze the papilledema from intracranial hypertension either functionally1 2 3 4 5 6 7 8 9 or morphologically.10 11 12 13 14 15 16 17 18 19 20 Among the functional techniques, electrophysiology of the optic nerve (pattern evoked potentials and pattern electroretinogram),2 5 7 pupil response testing,6 contrast sensitivity testing,1 3 8 9 automated threshold perimetry,3 4 8 9 motion perimetry,9 and high-pass resolution perimetry4 9 have been used. The prominent role of automated perimetry in detecting the earliest functional losses and following up the progression of dysfunction has been stressed by different studies.3 8 21 Morphologic techniques include ophthalmoscopic examination,11 fluorescein angiography,10 optic disc and retinal nerve fiber layer photography,9 15 stereoscopic color photography,10 echographic transverse optic nerve diameter measurements,12 13 computed tomography (CT),14 magnetic resonance imaging (MRI),20 and, recently, confocal scanning laser ophthalmoscopy (CSLO).16 17 18 19 In papilledema due to idiopathic intracranial hypertension (IIH), reliability of CSLO as a quantitative method of evaluating disc swelling has been demonstrated.17 18 19

The correlation between optic disc morphology and visual field sensitivity in papilledema has not been quantitatively determined, although qualitative associations have been reported.3 9 17 18 22 23 24 25 Establishing such a correlation could strengthen the diagnostic utility of both methods in diagnosis and follow-up of papilledema. The purpose of the present study was to evaluate whether, and to what extent, the degree of disc swelling, as measured by CSLO tomographic parameters, correlates quantitatively with the severity of visual dysfunction, determined by automated perimetry. To this end, correlations were evaluated in the same patients either cross-sectionally or longitudinally. The results show a close association between optic nerve tomography and visual field sensitivity in recently diagnosed papilledema.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 References
 
Subjects
The patients enrolled in the study were recruited from larger cohorts of patients evaluated at the Neuro-Ophthalmology Service of our institution. Both eyes of eight patients (four men, four women; mean age ± SD: 41.1 ± 12.3 years), with ophthalmoscopic evidence of a variable degree of disc swelling and a clinical diagnosis of IIH, were examined with both CSLO tomography and automated perimetry. Testing was performed at the time of diagnosis and at various times during a clinical follow-up of variable length (described later). The test schedule and demographic and clinical data are summarized in Table 1 . The diagnosis was based on the modified Dandy criteria, reported by Smith26 : signs and symptoms of increased intracranial pressure in an alert and awake patient, normal neurologic examination findings except for papilledema and its associated visual loss and sixth nerve palsies, normal findings in neurodiagnostic studies except for increased cerebrospinal fluid (CSF) pressure (>250 mm H2O), and no secondary cause of intracranial hypertension. All patients had normal neurodiagnostic evaluation by CT brain scanning and MRI. CSF pressure measured in patients by lumbar puncture ranged from 260 to 320 mm H2O. Direct ophthalmoscopic and 90-diopter (D) lens biomicroscopic assessment of the degree of papilledema was based on the staging scheme proposed by Frisén11 : the whole range of disc swelling from stage 0 (normal optic disc) to stage 5 (marked disc swelling) was represented in the patient group. None of them showed signs of atrophic papilledema, such as marked pallor, gliosis, and vessel attenuation. Additional inclusion criteria were good compliance, clear CSLO images of the optic nerve head (average variability <30 µm), reliable visual fields27 (at least two Humphrey 30-2 threshold tests [Allergan-Humphrey, San Leandro, CA] within 5 days), refractive errors comprised between -5.50 and +2.00 D spherical equivalent, astigmatism less than ± 1.00 D, and absence of other disorders affecting the optic disc or visual field. Best corrected visual acuity was 20/20 in all but one eye in one patient (20/30 in the left eye of patient 7, Table 1 ).


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  		Table 1. Demographic and Clinical Features of Patients

 
Patients were studied serially during the course of a follow-up period ranging from 5 to 30 months (mean ± SD: 17.1 ± 9). All patients were under medical treatment (oral acetazolamide, 500-1000 mg twice daily) during the follow-up, with temporary (<2 weeks) suspension periods. At each follow-up session, tomographic analysis was performed on the same day of the first perimetric examination by a different operator, masked as to the patient’s characteristics and clinical information. Sometimes, measurement sessions had to be limited to only one eye of a patient because of fatigue. Both the tomographic (Heidelberg Retinal Tomograph [HRT]; Heidelberg Engineering, Heidelberg, Germany) and field measurements were unavailable for the left eye of patient 4 at visit 3, whereas visual field data were unavailable for both eyes of patients 3 and 8 at visits 3 and 6, respectively; and for the left eye of patient 2 at visit 2. Informed consent was obtained from every patient, after the procedures to be used in the study were fully explained. The research followed the tenets of the Declaration of Helsinki.

Apparatus and Procedure
Optic disc morphometry was performed by means of the HRT by a trained operator (TS). Details of the instrument and its reproducibility have been published.18 28 29 30 31 32 33 34 35 36 A topography image was taken as a series of 32 two-dimensional transverse optic section images, acquired in approximately 1.6 seconds, each consisting of 256 x2 56 pixels (65,536 picture elements). In this study three 20° images were obtained for each eye, and the mean image of the three scans was used for the optic disc measurements, according to Weinreb et al.30 The scanning depth of each topographic image series ranged from 0.5 to 4.0 mm in 0.5-mm increments, depending on the individual degree of disc swelling. Each mean topography image was automatically corrected for horizontal and vertical tilt.37 HRT software (ver. 2.01; Heidelberg Engineering) calculated the stereometric parameters of the optic nerve head. Magnification errors were automatically corrected by using patients’ keratometry readings.37 A contour line was marked by the computer-generated circle outside the disc edema, according to a published procedure.17 18 34 Specifically, this circle was located on healthy, nonedematous retina, to avoid height measurement error by having a reference surface as flat as possible (the HRT curved surface38 ). For this purpose its mean radius was fixed to 2.5 mm for each eye—that is, along the extreme periphery of the image. The overall three-dimensional parameters, volume above surface (VAS), effective mean height (EMH), and maximum height in contour (MxHC), were automatically measured relative to the curved surface. EMH represents the mean height of all parts within the contour line that are located above the curved surface. MxHC is defined as the mean height of the 5% pixels with the highest height values within the contour line.37 Another axial boundary, the current standard reference plane,18 19 38 was used by the HRT software to determine the volume above reference (VAR).37 Volumetric parameters were also evaluated for the following predefined HRT disc sectors: superior (S, 90°), nasal (N, 90°), inferior (I, 90°), and temporal (T, 90°). Optic disc sector analysis was performed to evaluate the presence of a relationship between regional disc edema and functional loss at corresponding disc and field sectors.

Test–retest variability of the three measurements of each point, expressed by the average of the SDs of the topographic values of each pixel in the three images, was 17.84 ± 6.93 µm (range, 7.73–29.91) for right eyes and 19.59 ± 6.44 µm (range, 8.85–27.27) for left eyes.

Visual field analysis was performed on the Humphrey field analyzer model 630 (Allergan-Humphrey), using the 30-2 threshold test with evaluation by software provided by the manufacturer (STATPAC; Allergan-Humphrey). All patients were experienced in automated threshold perimetry, and results were analyzed beginning with the second visual field examination. To be considered reproducible, either at the study entry or during the follow-up, individual field defects had to be confirmed in at least two separate testing sessions performed within 5 days. In each patient, sensitivity loss at a given location was confirmed within ±2 dB. The locations of defects (Table 1) were confirmed within ± 6°. Intratest perimetric reliability was evaluated as fixation losses and false-positive and false-negative errors, according to Bickler-Bluth et al.27 Short-term fluctuation (SF) did not exceed the 2% range in each patient. When outside the normal range, SF depended on the individual degree of visual loss.

For data analysis, the global field sensitivity indices mean deviation (MD) and pattern SD (PSD) were used, and sectorial mean perimetric deviation was also calculated from the total-deviation plot, according to the method proposed by Kono et al.39 (Fig. 1) . More specifically, the Humphrey visual field was divided into four sectors (central, temporal, superior, and inferior) corresponding to the different quadrants of the HRT disc rim (temporal, nasal, inferior, and superior, respectively). This correspondence was related to the anatomic course of retinal nerve fibers to the optic disc.39 Visual field loss of the patients ranged from minimal to a marked degree, according to the scheme proposed by Wall and George.3



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  		Figure 1. Schematic representation of central visual field (Humphrey 30-2 threshold test) of a right eye, divided into four sectors corresponding to the different quadrants of the HRT disc rim, according to the anatomic distribution of optic nerve fibers38 : () perimetric central sector; () perimetric temporal sector; ({circ}) perimetric superior sector; and (•) perimetric inferior sector.

 
Statistical Analysis
HRT and perimetric results from the right eye of each patient, as well as the interocular differences in both HRT and perimetric values,9 were included in the statistical analysis. Correlations between tomographic and perimetric data obtained at baseline were evaluated by nonparametric Spearman’s correlation analysis. A Wilcoxon sign test for matched pairs was used to compare tomographic and perimetric measures obtained at baseline and after approximately 3 months of treatment. In all the analyses, two-tailed P <= 0.05 was considered significant.


   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 References
 
Cross-sectional Analysis
Individual tomographic and perimetric data, derived from global analysis at baseline, are reported in Table 2 . Some patients had a considerable degree of asymmetric papilledema (e.g., patients 1 and 7), as expressed by tomographic parameters, whereas in the remaining six, the degree of disc edema was similar in both eyes. Perimetric sensitivity losses expressed by MD and PSD tended to be systematically larger in eyes with a greater amount of disc edema. There were significant negative correlations between the individual tomographic values and the corresponding perimetric MDs obtained at baseline, either in the global or sectorial analysis (Spearman’s r <= -0.62). Correlations between the tomographic values and the perimetric PSD did not attain statistical significance, even though the trend was similar to that observed for the MD.


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  		Table 2. Morphometric and Perimetric Data from Patients at Baseline

 
Scatterplots of the individual Humphrey MD values as a function of the corresponding tomographic VAR and VAS parameters are shown in Figure 2 . Data obtained from global analysis and from the analysis of temporal and inferior disc sectors are reported. Linear regression lines are fitted to the data points. MD losses tended to be progressively greater in eyes with greater HRT values. In the temporal and inferior sectors, a topographic relationship between tomographic disc elevation and perimetric loss was observed. Correlations between volumetric and perimetric values at nasal and superior disc sectors also showed the same trend. The correlational analysis was performed again after excluding all the peripapillary locations (10 points adjacent to the blind-spot projection), to minimize the possible artifacts due to blind-spot enlargement.3 8 9 This new analysis (not shown in the Figure) provided very similar results.



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  		Figure 2. Perimetric mean deviation, obtained from right eyes of individual patients, plotted as a function of corresponding tomographic VAR and VAS parameters at baseline (global and sectorial disc analysis).

 
Most correlations recorded at baseline between interocular tomographic and perimetric differences (MD and PSD), for use in either global and sectorial analysis, were significant at P <= 0.05 (Spearman’s r <= -0.57 for MD, r >= 0.64 for PSD). Scatterplots of the individual intereye Humphrey MD difference values, plotted as a function of the corresponding volumetric differences are shown in Figure 3 . Data collected from the global analysis and from the analysis of the inferior disc sector are shown. Negative values of volumetric differences indicate that left eye discs were more edematous than right ones. Similarly, for MD differences, positive values indicate that left eyes were more functionally damaged than right ones. It is apparent from scatterplots of Figure 3 that interocular tomographic differences were associated in both entity and direction to the corresponding perimetric differences.



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  		Figure 3. Interocular perimetric MD difference values, recorded from individual patients, plotted as a function of the corresponding interocular tomographic differences in VAR and VAS at baseline (global and inferior disc sector analysis).

 
Longitudinal Analysis
In Figure 4 , examples of HRT reflectance images obtained at baseline and at different times during the follow-up from the right eye of a patient with papilledema from IIH (patient 1; Table 1 ) are shown. Disc edema z-profiles, taken along vertical meridians (indicated by the thick lines) crossing both poles, are shown for each image. In the same figure, perimetric results of the tested eye, obtained at corresponding follow-up times, are also reported. The figure shows that during the follow-up period, there was a decrease of disc edema (as shown by the changes in the VAR and VAS values) that was paralleled by an improvement of visual field indices (MD and PSD).



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  		Figure 4. (A) HRT reflectance images of the optic disc swelling obtained (from top to bottom) at baseline and at different times (5 and 14.5 months) during the follow-up from a representative patient’s eye (right eye of patient 1 in Table 1 ). To the right of each image, the corresponding vertical z-score profiles (taken along vertical meridians and crossing both poles) are also shown. (B) Automated visual field measurements (total deviation plots from Humphrey 30-2 threshold test) obtained at the corresponding follow-up times.

 
Figure 5 shows the tomographic VAS and perimetric MD individually recorded at various times over the follow-up period. Data are separately plotted for right and left eyes. After medical treatment, the VAS declined rapidly in most patients, indicating a trend toward regression of disc edema. In parallel with the decline in the VAS, perimetric MD tended to move toward normal values at comparable follow-up times.



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  		Figure 5. Tomographic VAS and perimetric MD serially recorded during the follow-up period from right and left eyes of individual patients. Dotted lines: missing data points at one visit.

 
Box plots of volumetric and perimetric values recorded from the right eyes of patients at baseline and after approximately 3 months of follow-up are shown in Figure 6 . A Wilcoxon sign test showed that volumetric values significantly decreased (VAR, z-score: -2.38, P = 0.017; VAS, z-score: -2.52, P = 0.012), whereas perimetric MD increased (z-score: 2.24, P = 0.025) at comparable follow-up times. Perimetric PSD changes were not statistically significant.



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  		Figure 6. Box plots of VAR and VAS and perimetric MD and PSD recorded from the right eyes of patients at baseline and after approximately 3 months of follow-up. Box shows 75th, 50th, and 25th percentiles. Error bars show 99th and 1st percentiles.

 

   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
Studies evaluating the correlation between degree of papilledema and visual field loss have reported different and, at least in part, conflicting results (see Table 3 ).3 9 17 18 22 23 24 25 Although a qualitative correlation between high-grade papilledema and perimetric loss has been found by some investigators,3 23 24 it has been suggested that the severity of visual field loss in individual patients cannot be predicted from the severity of papilledema.3 25 Göbel et al.17 did not find any quantitative correlation between HRT measurements of disc swelling and automated field sensitivity. More recently, Mulholland et al.18 reported that, in individual patients with IIH, changes in CSLO disc volume were qualitatively correlated with corresponding perimetric sensitivity changes in the short term. However, no quantitative correlations were reported, either in cross-sectional or longitudinal measurements. Wall and White,9 evaluating patients with IIH who had asymmetric papilledema, found a significant correlation between visual field sensitivity loss and papilledema grade, evaluated on optic disc photographs according to the Frisén scheme.11 The strength of the correlation was partially weakened by a large interindividual variability, so that r was much greater when the fellow eyes of several patients were compared.


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  		Table 3. Qualitative Correlations between Degree of Papilledema and Visual Loss in the Literature

 
In the present study, correlations between morphometric CSLO parameters and perimetric indices MD and PSD were evaluated either cross-sectionally or longitudinally in a group of patients with recently diagnosed papilledema associated with IIH. This sample of patients, because it was equally distributed between males and females, may not be representative of IIH, a disease more prevalent in females.21 However, the purpose of this study was to analyze these correlations in papilledema and not in IIH. In addition, the patients included in the study had reliable visual fields with a relatively high reproducibility of their defects. Test–retest variability of perimetric sensitivity usually represents a major concern when evaluating changes over time in patients with early field losses.40 The good reproducibility found in this patient sample allowed morphofunctional correlations to be evaluated with a low degree of noise.

The results showed that, at baseline evaluations, there was a significant negative correlation between the disc volume and height and the perimetric MD measurements. Interocular analysis confirmed these findings and showed agreement with the data of Wall and White.9 The correlations showed a topographic specificity—that is, regional localized edema was associated with sensitivity losses at corresponding field sectors. As far as we know, this is the first report to evaluate such a topographic relationship in papilledema. In the follow-up period, the optic disc volumetric changes appeared to be accompanied by corresponding perimetric variations. In this study, patients with advanced disc-swelling phases were excluded, because irreversible axonal damage might hinder the correlation between disc morphology and perimetry.

The correlations between papilledema grade and functional losses, as well as the trends observed over the follow-up period, lend support to the hypothesis that both techniques can be used to monitor the amount of disc edema and the effectiveness of treatments aimed at reducing intracranial hypertension. In papilledema, perimetric loss is thought to result from elevated tissue pressure within the optic nerve due to the increased CSF pressure transmitted through optic nerve sheaths.41 42 Of the two types of field loss resulting from disc edema, the blind-spot enlargement and the nerve fiber–related visual field defects, the former is considered to be artifactual, being a consequence of edema-induced local hyperopia, photoreceptor misalignment, or both,3 8 43 whereas the latter are commonly accepted as the primary indication of damage to the axons of retinal ganglion cells.8

It cannot be excluded that both types of defects may correlate with the amount of papilledema recorded in individual patients. However, a correlational analysis, performed on the patients’ right eyes after excluding thresholds measured at all the peripapillary locations, provided results very similar to those of the original analysis. In addition, there are reasons to suspect that a specific correlation between nerve fiber–related visual defects and the degree of edema may hold, at least in patients such as the one reported in Figure 4 , in whom the right eye showed at baseline a typical inferonasal nerve fiber defect that could not have been ascribed to blind-spot enlargement. Significant improvement of the field defect in this patient was mirrored by a regression of edema in the topographically corresponding superior sector of the optic disc. Although this sectorial association supports the relationship of localized axonal damage with corresponding perimetric abnormalities, further studies on a large cohort of patients are needed to clarify this issue.

In this patient sample, CSLO assessment was always performed on 20° images, unlike the procedures used by Göbel et al.17 and Mulholland et al.,18 thus providing a more homogeneous sample of data while minimizing artifactual values. Furthermore, analysis of volumetric measurements by using both VAS and VAR parameters may result in a more accurate estimate of the amount of disc edema, compared, for instance, with that reported by Mulholland et al. This is supported by two different pieces of evidence. First, the VAR reference plane is derived from only a very small (temporal 6°) portion of the contour line,18 19 38 which makes sense in glaucoma studies, but does not appear very meaningful for quantifying disc edema. Even small edematous retinal areas under the contour line in the temporal segment may largely underestimate the papilledema, especially for follow-up evaluations. By contrast, the use of the whole circumference to assess a reference surface (the HRT curved surface38 used for the VAS measurement) may compensate mild contour line height variations and minimize measurement errors. Second, the use of the VAS parameter was suggested by previous reports in which its accuracy and reproducibility were evaluated in the presence of retinal elevations.17 32 34

In conclusion, in the present findings in recently diagnosed papilledema, morphometric abnormalities were quantitatively associated with perimetric threshold alterations. Reversibility of functional damage also appeared to occur in parallel with disc-swelling resolution. Taken together, the data further support the use of the HRT technique as a noninvasive, quantitative method of monitoring the amount and evolution of papilledema, as well as of evaluating the effects of treatments.


   Footnotes
 
Submitted for publication August 9, 2000; revised February 5, 2001; accepted February 28, 2001.

Commercial relationships policy: N.

The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.

Corresponding author: Tommaso Salgarello, Istituto di Oftalmologia, Università Cattolica S. Cuore, Lgo F. Vito 1, 00168 Rome, Italy. tsalgarello{at}hotmail.com


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 

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