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Laser Scanning Tomography of the Optic Nerve Head in a Normal Elderly Population: The Bridlington Eye Assessment Project

¹From the Department of Ophthalmology, Queen’s Medical Centre, University Hospital, Nottingham, United Kingdom; and ²The Medical Centre, Bridlington, United Kingdom.

	Abstract

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PURPOSE. To assess optic nerve head topographic parameters using the Heidelberg Retina Tomograph (HRT) II (Heidelberg Engineering GmbH, Dossenheim, Germany) in a normal elderly population.

METHODS. Optic nerve head analysis of 918 eyes of 459 normal elderly patients was performed. All patients were consecutive in a cohort screened for eye disease. Normal subjects were defined with a normal visual field on automated suprathreshold screening, intraocular pressure less than 22 mmHg, and minimum corrected visual acuity of 6/12. All optic discs were contoured by two investigators and the mean parameters analyzed. The effects of age, sex, and disc size were assessed.

RESULTS. Subjects’ (262 women and 197 men) mean age was 72.6 ± 5.1 (SD) years (range, 65.5–89.3). Mean ± SD global disc area, cup/disc area ratio, and neuroretinal rim area were 1.98 ± 0.36 mm², 0.22 ± 0.14, and 1.52 ± 0.31 mm², respectively. Disc area did not differ significantly based on eye side or sex. The women were found to have a significantly larger rim volume, mean retinal nerve fiber layer (RNFL) thickness, and cross-sectional area than the men and tended to have smaller cup areas/volumes and cup/disc area ratios. Most tomography parameters were found to be significantly influenced by disc size.

CONCLUSIONS. To the authors’ knowledge, this is the first large study of optic nerve head parameters in the elderly normal population using the HRT II. This age range is particularly relevant to glaucoma detection and pertinent to discriminant analyses separating normal subjects from glaucoma in screening for the disease. Given the systematic differences between the parameters in men and women, reference ranges should be quoted by sex.

	Methods

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Subjects: The Bridlington Eye Assessment Project
The methodology of the Bridlington Eye Assessment Project has not been described previously and is therefore detailed herein. As just stated, the project systematically invited all the town of Bridlington’s elderly population (over the age of 65 years) for a comprehensive screening eye examination by one of four trained optometrists. Patients aged 65 or older on May 11, 2002, and registered with a general practitioner in Bridlington were eligible to attend the examination. Patients known to be registered as blind or partially sighted, bed-bound or demented, or moving into or out of the area during the study were excluded. The Project saw it’s first patient on May 11, 2002, and had seen 1246 patients when this study commenced in January 2004. Informed consent was obtained from all participants, and a local research ethics committee approved all methodology. All methods adhered to the guidelines of the Declaration of Helsinki for research in human subjects.

A relevant standardized medical history was obtained (diabetes, stroke, hypertension) together with the patient’s drug history. Distance and reading spectacle requirements were noted in addition to any history of amblyopia, ocular surgery, or any other ocular disease. Specifically, any history of glaucoma, diabetic retinopathy, or macular degeneration was noted. Family history of glaucoma was determined, together with the patient’s driving status and social circumstances. Uncorrected, corrected, and pinhole logMAR (logarithm of the minimum angle of resolution) visual acuity was then obtained (Bailey-Lovie no. 4 Chart; National Vision Research Institute of Australia, Carlton, Victoria, Australia). The patient was then examined by one of four optometrists trained specifically for the project. Standardized slit lamp examination of the anterior segment and Goldmann applanation tonometry were performed. After instillation of dilation drops, automated visual field analysis was performed with a perimeter (Henson Pro 5000) with software version 3.1.4 (Tinsley Instruments, Croydon, UK). A single-stimulus, suprathreshold, central 26-point test was used. This was automatically extended to a 68-point test if a defect was detected. The patient’s lens, optic disc, macula, and peripheral retina were then specifically examined by slit lamp biomicroscopy with 90-D lens. Decisions on appropriate further management of the patient were made before high-resolution digital fundus photographs (TRC NW6S; Topcon, Tokyo, Japan) and HRT II images (HRT II software ver. 1.4.1.0; Heidelberg Engineering GmbH) were obtained.

Confocal Scanning Laser Ophthalmoscope Assessment
In this study, data from the first 1246 patients were examined. Of those, 576 patients were defined as normal for the purposes of this study with an intraocular pressure less than 22 mm Hg in both eyes, a normal visual field determined by suprathreshold automated examination, and corrected logMAR acuity of at least 0.3 (Snellen equivalent 6/12). Patients with a history of glaucoma or use of ocular pressure-lowering treatment were excluded. Of the 576 normal patients, a further 16 were excluded because of absent or unacceptable disc images. A further 10 patients were excluded because splinter hemorrhages were observed clinically on one or both of their optic discs. Patients were purposely not excluded on the basis of an optic disc clinically suspected of glaucoma. Patients were imaged with HRT II, with the scanner’s focus being adjusted according to the patient’s refraction and to obtain the best image. The optic disc contour line was drawn by two investigators (GA, MJH) to mark the edge of the optic disc. Contour lines were placed on separate database copies so that each investigator could not see the contour line drawn by the other. HRT II then calculated disc area (square millimeters) and 12 further stereometric parameters. The parameters were cup area (square millimeters), rim area (square millimeters), cup-to-disc area ratio, rim-to-disc area ratio, cup volume (cubic millimeters), rim volume (cubic millimeters), mean cup depth (millimeters), maximum cup depth (millimeters), height variation contour (millimeters), cup shape measure, mean retinal nerve fiber layer (RNFL) thickness (millimeters), and RNFL cross-sectional area (square millimeters). Each of these parameters was expressed for the global disc and for six individual disc sectors (temporal, temporal superior, temporal inferior, nasal, nasal superior, and nasal inferior). The average variability (SD) of the three HRT images comprising the mean topographic image was 34 µm. Because of the large range of average variability (0–258 µm) discs with the largest 10% of average variability were excluded on a patient-wise (eye pair) basis (a further 91 patient exclusions). The maximum average variability was then 68 µm, with a mean ± SD of 26.8 ± 13.3 µm. This was comparable to previous investigations and gave acceptable data quality for the purposes of generating a reference range.⁵

Analysis
HRT II parameters for this study were derived as a the mean of parameters generated by the two individual investigators. Contour line placement is based on subjective judgment and inevitably generates intrinsic variability. Using the mean parameter value attempts to reduce this variability, improving the applicability of the results beyond the individual investigator. Investigator agreement and the effects of using a digital photographic image to aid contour placement are to be the subject of a further communication.

ONH HRT II parameters were analyzed on computer (SPSS for Windows, ver. 12.0, Statistical Package for Social Sciences; SPSS, Inc., Chicago, IL). Parameter indices were assessed visually for normality by using histograms and objectively with the Kolmogorov-Smirnov test. As expected, all parameters produced a bell-shaped distribution, apart from those related to the cup area and volume (which has a minimum value of zero and is not therefore normally distributed). Nearly all parameters with a bell-shaped distribution showed significant departure from normality with the Kolmogorov-Smirnov test. For this reason, and because parameter comparisons could not be truly classified as paired or independent, the Mann-Whitney test was used to assess the significance of differences in parameters between right and left eyes and between the men and women. Two-tailed tests were used throughout. With a large dataset that was not found to be normally distributed, we state the 95th and 99th percentile limits of normality (reference range) for our data.

Linear regression analysis was used to determine which variables were related to disc area. In no case was R² greater than 0.37. Thus, with relatively small dependent effects, and non-normally distributed data, we quote Spearman’s rank correlation to assess the relative effects of disc area on disc parameters. The effect of age on global disc parameters was assessed with the Kruskal-Wallis test by dividing the sample into quartiles based on age. Statistical significance for this study was set at the 5% level. However, for multiple comparisons among the 12 HRT parameters, a Bonferroni correction was applied with resultant significance at P < 0.004.

	Results

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Demographics
A total of 918 eyes of 459 patients were included in the study. All patients were white and of European extraction. The mean age of the subjects (262 women and 197 men) was 72.6 ± 5.1 (SD) years (range, 65.5–89.3). The mean age of the men and women was not significantly different (72.9 and 72.4 years, respectively; P = 0.41). Of those patients who were excluded 57.0% were women. The mean age of excluded patients was significantly higher than that of those who were included (75.0 vs. 72.6 years; P < 0.0001).

ONH Parameters
The mean disc area was 1.98 ± 0.36 mm² (SD). The mean, SD, median, and 2.5th/97.5th and 0.5th/99.5th percentiles for all global parameters are presented in Table 1 . Global disc area showed a bell-shaped distribution with a degree of positive skew. As expected, global cup area, and all cup-related variables did not show bell-shaped distributions (Fig. 1) .

View larger version (16K): [in this window] [in a new window]   FIGURE 1. Global disc area and global cup area distribution in 918 eyes of 459 normal elderly patients.

View larger version (15K): [in this window] [in a new window]   FIGURE 2. Changes in global rim/disc area ratio between the four age quartile groups of 918 eyes of 459 normal elderly patients.

	Discussion

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We demonstrated consistent differences in ONH parameters between the sexes. In our study, the women had significantly greater rim volume, mean RNFL thickness, and cross-sectional area and tended to have a smaller cup area and volume and cup/disc area ratio. There was no significant difference in mean age between the men and the women, to account for the observed differences. The sex-related differences in cup-related parameters did not reach statistical significance, although nonparametric tests with a Bonferroni correction return a conservative result (increasing the risk of type II errors).¹⁹ We note that analyses performed using the unpaired Student’s t-test (equality of variances not assumed) returned significant differences between the sexes for all cup- and rim-related variables at the 0.5% level. Hermann et al.⁹ found that rim volume was significantly greater in the right eye in women than in men, though they found no other significant differences between the sexes. Our data did not reproduce this finding. Other studies have found no significant difference in parameters based on sex.^{20 21 22} In contrast to our data, using digitized photographic optic disc images, Rudnicka et al.²³ found women to have smaller rim areas and larger cup areas (differences of marginal statistical significance). Using stereoscopic optic disc images, Ramrattan et al.²⁴ found men to have significantly larger disc area and rim area. These variations are not due to racial factors, as nearly all subjects in these studies were white. The mean age of subjects in many of these studies was considerably lower than in our sample. Given that elderly men have twice the prevalence of open-angle glaucoma than do women,¹⁴ our findings of smaller rim volumes and tendency to larger cup-related measurements in the men than in the women may reflect the progression of a greater proportion of men toward glaucoma. Having found significant sex-related differences, for the purposes of using our data to distinguish normal and glaucoma, we state sex-specific normal ranges for HRT II ONH parameters.

Our study found significant differences between right and left eyes in height variation contour and cup shape measure. When we examined the effects of laterality for each sex, cup shape measure differed significantly only in the men, and height variation contour differed significantly only in the women. These differences, however, were small and of little clinical significance. A recent study found no systematic differences based on laterality,¹⁰ previous studies having found conflicting differences in mean RNFL thickness and cross-sectional area that were clinically minimal.^{9 12} To date, no consistent differences in ONH parameters based on laterality have been demonstrated.

Although rim and nerve-fiber–related measurements tended to decrease with age, we did not find a significant effect of age on ONH parameters in our study. However, with a minimum age of 65 years, it is likely that our sample lacks power to detect a significant effect without younger patients for comparison. Using image analysis of stereoscopic disc photographs, another population-based study with a minimum age of 55 also detected no age effect on ONH parameters.²⁴ Studies with a larger age range have detected significant enlargement of cup measurements, with reduction in rim/nerve fiber layer measurements with increasing age.^{9 10 11} In common with previous studies, we have also shown many ONH parameters to be dependent on disc size.^{5 10 11} We found height variation contour to be the only parameter independent of disc area. Cup shape measure, which Durukan et al.¹⁰ found to be independent of disc area, had a significant association with disc area in our study. Although cup shape measure has shown promise in detecting glaucoma and its progression,^{25 26} any variability due to disc area widens the confidence limits of normality.

Heidelberg Engineering recommends that images of low quality (SD of the mean topographic image greater than 50 µm) should not be used in a follow-up (change) analysis. Even by excluding 10% of patients with the greatest SD, the maximum SD in our sample was 68 µm. Although this should be considered a limitation of our study, it is not unexpected in our sample with a minimum age of 65 years. Previous studies have found that image variability increases with age²⁷ and with the presence of cataract,²⁸ though the effect of cataract was much reduced by acquiring images through a dilated pupil. If we were to exclude patients with SDs over 50 µm, we would preferentially exclude more elderly patients, and limit one of the main novelties of our study as an analysis of HRT II imaging in the elderly. We have included patients on an eye-pair basis. Thus, we would lose a significant number of patients (120 eyes in 60 patients further excluded) if we excluded them because even one eye had an SD over 50 µm. We therefore excluded patients with the greatest 10% of image SD, to remove outlying patients with SDs not representative of the group as a whole. When we reanalyzed the sample, with patients with an SD over 50 µm excluded, all global parameter means and SDs remained essentially unchanged, with no significant differences caused by the new exclusion criterion. We anticipate that, in a cross-sectional study, the effect of mean topographic image SD is less critical than in longitudinal studies, due to the principal of regression to the mean. In our study only one mean topographic image was acquired per eye. The focusing dial of the machine was adjusted according to the patients’ refraction and to obtain the clearest image. Much of the acquisition process of the HRT II is automated. If the machine stated that astigmatism was significantly impairing the image, then the image was obtained through the patients’ spectacles. If the image acquired was visually unacceptable, then the process was repeated to obtain an acceptable image, although this was not possible in a few patients. The causes of poor image quality are important, especially in this age group, for the reasons we have outlined. It is possible that the use of drops before the test and applanation tonometry reduced image quality. However, tonometry was performed before dilation, and HRT II image acquisition was not performed until at least 20 minutes after instillation of drops. The effects are therefore likely to have been minimal. The relationship between image SD and patient variables in our sample is to be the subject of a further communication.

Of the 1246 patients examined by BEAP, our definitions of normality have excluded most. This limitation of our study arises mainly from the lack of best-corrected visual acuity obtained with a contemporary refraction and a large number of false-positive suprathreshold visual field tests. In this elderly age group, false-positive field results are common and represent a major hindrance to the use of visual field tests in screening for glaucoma. In our study, individual reading glasses were used when available. Otherwise, based on focimetry of the patient’s spectacles, the optometrist recommended a spherical reading "add" (wide-lens spectacles) to be worn while the patient performed the test. All patients had received mydriatics before performing the visual field test. Although the effect of mydriasis is not expected to be uniform, in this elderly age group, dilation reduces the effect of senile miosis on the visual field tests—especially relevant in the presence of cataract. With the minimum age of 65 years in our sample conferring significant presbyopia, we would not anticipate significant variability effect due to reduced accommodation because of mydriasis. Overall, the visual field test conditions are likely to have produced some false-positive, abnormal findings, resulting in exclusion from the study. However, even with many exclusions of potentially "normal" patients, our data provide a reference range of normality for HRT II parameters drawn from a population-based sample with an age range relevant to glaucoma. Whether this new reference range, including both eyes of normal subjects, can improve discrimination between normal and glaucomatous eyes is to be the subject of a further communication.

	Acknowledgements

 
The authors thank Sheila MacNab (Project Manager), and Stephen Brown, Janet Button, Graham Langton, and Mark Kunz (Optometrists) for their work with the Project; John Bapty, Nigel Connell, Peter Jay, and Gillian Poole for their work as the charity trustees of the Bridlington Eye Assessment Project; and David P. Crabb (Lecturer in Statistics, School of Science, The Nottingham Trent University, Nottingham, UK) for assistance with statistical analyses.

	Footnotes

 
Supported by an unrestricted grant from Pfizer to the Bridlington Eye Assessment Project and by Pharmacia, Yorkshire Wolds and Coast Primary Care Trust, The Lords Feoffees of Bridlington, Bridlington Hospital League of Friends, The Hull and East Riding Charitable Trust, The National Eye Research Centre (Yorkshire), The Rotary Club of Bridlington, The Alexander Pigott Wernher Memorial Trust, Bridlington Lions Club, The Inner Wheel Club of Bridlington, Soroptimist International of Bridlington, and The Patricia and Donald Shepherd Charitable Trust.

Submitted for publication January 25, 2005; revised February 28 and March 14, 2005; accepted March 29, 2005.

Disclosure: S.A. Vernon, None; M.J. Hawker, Pfizer (F); G. Ainsworth, None; J.G. Hillman, None; H.K. MacNab, None; H.S. Dua, None

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: Stephen A. Vernon, Department of Ophthalmology, Queen’s Medical Centre, University Hospital, Nottingham NG7 2UH, UK; stephen.vernon{at}qmc.nhs.uk.

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This Article Abstract Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (15) Citing Articles via Google Scholar Google Scholar Articles by Vernon, S. A. Articles by Dua, H. S. Search for Related Content PubMed PubMed Citation Articles by Vernon, S. A. Articles by Dua, H. S.