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Incidence and Rates of Visual Field Progression after Longitudinally Measured Optic Disc Change in Glaucoma

Balwantray C. Chauhan, PhD, Marcelo T. Nicolela, MD, Paul H. Artes, PhD

Objective: To determine whether glaucoma patients with progressive optic disc change have subsequent visual field progression earlier and at a faster rate compared with those without disc change. Design: Prospective, longitudinal, cohort study. Participants and Controls: Eighty-one patients with open-angle glaucoma. Methods: Patients underwent confocal scanning laser tomography and standard automated perimetry every 6 months. The complete follow-up was divided into initial and subsequent periods. Two initial periods--first 3 years (Protocol A) and first half of the total follow-up (Protocol B)--were used, with the respective remainder being the subsequent follow-up. Disc change during the initial follow-up was determined with liberal, moderate, or conservative criteria of the Topographic Change Analysis. Subsequent field progression was determined with significant pattern deviation change in 3 locations (criterion used in the Early Manifest Glaucoma Trial). As a control analysis, field change during the initial follow-up was determined with significant pattern deviation change in 1, 2, or 3 locations. Main Outcome Measures: Survival time to subsequent field progression, rates of mean deviation (MD) change, and positive and negative likelihood ratios. Results: The median (interquartile range) total follow-up was 11.0 (8.0 ­12.0) years with 22 (18 ­24) examinations. More patients had disc changes during the initial follow-up compared with field changes. The mean time to field progression was consistently shorter (protocol A, 0.8 ­1.7 years; protocol B, 0.3­ 0.7 years) in patients with prior disc change. In the control analysis, patients with prior field change had statistically earlier subsequent field progression (protocol A, 2.9 ­3.0 years; protocol B, 0.7­ 0.9). Similarly, patients with either prior disc or field change always had worse mean rates of subsequent MD change, although the distributions overlapped widely. Patients with subsequent field progression were up to 3 times more likely to have prior disc change compared with those without, and up to 5 times more likely to have prior field change compared with those without. Conclusions: Longitudinally measured optic disc change is predictive of subsequent visual field progression and may be an efficacious end point for functional outcomes in clinical studies and trials in glaucoma. Financial Disclosure(s): The authors have no proprietary or commercial interest in any of the materials discussed in this article. Ophthalmology 2009;116:2110 ­2118 © 2009 by the American Academy of Ophthalmology.

Progressive optic disc and visual field changes are features of advancing glaucoma. Determining whether structural changes occur before functional ones (or vice versa) is important for providing clinicians with guidelines on the optimal follow-up of patients and with indications for earlier or different treatment interventions for better outcomes. However, to resolve the temporal sequence of structural and functional changes, the existence of an underlying relationship between these expressions of disease progression is assumed. Recent evidence from prospective longitudinal studies has shown the relative independence of optic disc and visual field change in glaucoma,1­3 whereas the recent, randomized, clinical trials in ocular hypertension and glaucoma have shown that visual field end points are reached first by some patients and optic disc end points are reached first by others.4 ­ 6 Newer diagnostic devices for imaging the optic disc, such as confocal scanning laser tomography (CSLT)7 have

been in clinical use for over a decade. In addition to performing diagnostic analysis of images obtained at 1 point in time,8 ­11 there are several methods for analyzing serial images to detect changes in optic disc topography over time.12­14 Increasing evidence suggests that these automated techniques perform at least as well as expert evaluation of conventional disc photographs15­18 and often better.15,17 However, even though early progressive optic disc changes can be detected, the consequences of these changes on visual function are not known. If CSLT-detected progressive changes in the optic disc predict earlier or more likely subsequent visual field progression, then important prognostic insight may be gained, with potential implications for clinical trial design. This study was conducted to answer whether open-angle glaucoma patients with progressive optic disc change measured with a range of criteria for defining change with CSLT were more likely to show earlier or faster subsequent visual

ISSN 0161-6420/09/$­see front matter doi:10.1016/j.ophtha.2009.04.031

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© 2009 by the American Academy of Ophthalmology Published by Elsevier Inc.

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Figure 1. Example of the division of the follow-up (in this case, 11 years) into initial and subsequent follow-up periods. In protocol A the initial follow-up was always 3 years, whereas in protocol B it was half of the entire follow-up (in this case, 5.5 years). In the test analysis, the initial follow-up was analyzed with confocal scanning laser tomography (CSLT) and the subsequent follow-up was analyzed with standard automated perimetry (SAP). In the control analysis, both the initial and subsequent follow-up were analyzed with SAP.

field progression compared with those without optic disc change.

Methods

Patients

The study participants were patients followed prospectively in an investigation on functional and structural changes in glaucoma with a variety of diagnostic tools. Patients were recruited consecutively from the glaucoma clinics of Capital Health District Authority, Halifax, Nova Scotia, Canada. Inclusion criteria were: (1) clinical diagnosis of open-angle glaucoma with notching or progressive thinning of the neuroretinal rim; (2) baseline visual field mean deviation (MD) between 2 and 10 dB; (3) open angles by gonioscopy; (4) best corrected visual acuity 6/12; and (5) 5 years follow-up. Exclusion criteria were: (1) systemic disease or systemic medication known to affect the visual field; (2) refractive error exceeding 5 diopters (equivalent sphere) of myopia or hyperopia, or 3 diopters of astigmatism; (3) contact lens wear; and (4) concomitant eye disease. If both eyes were eligible, 1 eye was randomly chosen as the study eye. In accordance with the Declaration of Helsinki, patients gave informed consent to participate in the study and the protocol was approved by the Capital Health Research Ethics Board with periodic review.

Data Collection and Processing

After enrolment, patients underwent baseline testing with CSLT and standard automated perimetry (SAP), and thereafter at 6-month intervals. Several CSLT images of the optic disc were obtained with the Heidelberg Retina Tomograph (Heidelberg Engineering GmbH, Heidelberg, Germany) with the 10° scan angle. Image quality was examined for illumination, optic disc centration within the image frame, and fixation stability. Three of the best quality images were then used to compute the mean topography image. Serial images were aligned with the Heidelberg Retina Tomograph 3 software (Heidelberg Engineering GmbH) and checked manually for good alignment. Poor quality and misaligned images were removed and the whole series reprocessed. This was necessary in 5% of the images. The contour line demarking the optic disc boundary in the baseline image was exported to the follow-up images. We performed SAP with the full-threshold 30-2 program of the Humphrey Field Analyzer (Carl Zeiss Meditec, Dublin, CA) with the Goldmann size III stimulus.

Statistical Analysis

The complete follow-up was split into an initial and subsequent follow-up with the objective of determining how change during the

initial follow-up predicted visual field progression during the subsequent follow-up. Two initial follow-up periods for analysis with CSLT were used: (1) first 3 years (protocol A) and (2) first half of the total follow-up (protocol B), with the respective remainder of the follow-up used for analysis with SAP (Fig 1). This was termed the test analysis. Change in the optic disc during the initial follow-up for each protocol was determined with the Topographical Change Analysis (TCA)12 of the Heidelberg Retina Tomograph. The TCA is an event-based technique for detecting changes in the optic disc and has been described in detail elsewhere as well as its comparison with conventional disc photographs.15,16,18,19 Briefly, based on an analysis of variance, the TCA takes into account the size and depth of the largest contiguous area or cluster of significant change within the optic disc border compared with the baseline image in 3 of 4 consecutive examinations. The 3 criteria for optic disc change were liberal, moderate, and conservative, estimated to yield false-positive rates of change of 19%, 6%, and 3% respectively, derived at the 5-year point in normal subjects followed identically.15 The liberal criterion required a significant cluster of 0.5% of the disc area and a depth change of 20 m; the moderate criterion a significant cluster of 1% of the disc area, and a depth change of 50 m; and the conservative criterion a significant cluster of 2% of the disc area and a depth change of 100 m. Subsequent visual field progression was determined with the event-based pattern deviation change probability analysis with customized software for full threshold data,20 and the trend-based rate of MD change (in dB/yr). These analyses are incorporated into the Glaucoma Progression Analysis of the Humphrey Field Analyzer Statpac software and have been detailed elsewhere.21 Briefly, for the event-based analysis, the difference in pattern deviation (difference in threshold from age-matched normal value and corrected for the general height of the visual field) between the baseline and each follow-up examination at each point is flagged as changed if it exceeds the expected limits of variability. The mean of the 2 visual fields immediately after 3 years of follow-up (protocol A) and immediately after half the total follow-up (protocol B) were defined as the baseline visual fields. To determine whether progression had occurred during the subsequent follow-up after the initial follow-up with CSLT, we used the criteria employed by the Early Manifest Glaucoma Trial (EMGT)22 requiring significant change in 3 points in 3 consecutive follow-up visual fields. In addition, subsequent rates of MD change for each protocol were computed with regression analysis. A control analysis was conducted to determine whether visual field change during the initial follow-up was more or less predictive of subsequent visual field progression compared with optic disc change during the initial follow-up. Protocols A and B were employed identically; however, for the initial follow-up, SAP was substituted for CSLT using the same analyses described for pattern

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Table 1. Follow-up Statistics* for Protocols A and B in the Test and Control Analyses

Initial Follow-up Protocol Test analysis A B Control analysis A B Follow-up (yrs) 3.0 (3.0­3.1) 5.5 (4.0­6.0) 3.0 (2.9­3.1) 5.5 (4.0­6.0) No. of Examinations 6 (6­7) 10 (8­12) 7 (7­7) 11 (9­13) Subsequent Follow-up Follow-up (yrs) 7.8 (5.0­8.8) 5.3 (4.0­5.8) 7.8 (5.0­8.8) 5.3 (4.0­5.8) No. of Examinations 15 (10­18) 11 (9­12) 15 (10­18) 11 (9­12)

*Median (interquartile range). Initial follow-up was with confocal scanning laser tomography in the test analysis and standard automated perimetry in the control analysis. Subsequent follow-up was with standard automated perimetry in both test and control analyses.

deviation change for 1, 2, and 3 points during the initial follow-up. The time to visual field progression during the subsequent follow-up was analyzed by Kaplan­Meier survival analysis. Groups were stratified according to whether, during the initial follow-up, there was change in the optic disc (test analysis) or visual field (control analysis). Group differences in survival time were compared with the log-rank test. Positive and negative likelihood ratios for findings during the initial follow-up for visual field progression during the subsequent follow-up were computed for the test and control analyses. Depending on the distribution of variables, means and standard deviations, or median and interquartile ranges were reported. Group comparisons were made with the Mann­Whitney test.

Results

There were 81 patients who qualified for the study. The median (interquartile range) age and total follow-up was 59.0 (51.2­ 69.2) and 11.0 (8.0 ­12.0) years, respectively. The length of follow-up and number of CSLT and SAP examinations for each protocol in the test and control analysis are shown in Table 1. The mean ( standard deviation) MD at baseline was 5.21 3.43 dB, and at the beginning of the subsequent visual field follow-up in protocols A and B was 5.99 3.98 and 6.14 4.63 dB, respectively. The number of patients who showed optic disc change during the initial follow-up for the 3 TCA criteria are shown in Table 2. More patients showed optic disc change during the initial follow-up in protocol B than protocol A because of the longer initial follow-up (by a median of 2.5 years). Similarly in the control analysis, more patients showed visual field change during the initial follow-up for both criteria in protocol B compared with protocol A. Survival curves for subsequent visual field progression depending on whether optic disc change during the initial follow-up period had occurred with the liberal, moderate, or conservative criterion for protocol A are shown in Figure 2. In each of these analyses, the mean survival time was shorter in patients with optic disc change than in those without, with the differences in mean survival time ranging from 0.8 to 1.7 years. Despite the consistency of these findings, the group differences in survival time failed to reach statistical significance (P 0.05; log-rank test). Similar patterns were observed in protocol B (Fig 2), where the initial follow-up with CSLT was longer but the subsequent follow-up with SAP was shorter. Patients with optic disc change during the initial follow-up had shorter mean survival times com-

pared with those without disc change, with the differences in mean survival time ranging 0.3 to 0.7 years. For the liberal or moderate TCA criteria, the differences in survival times were not significantly different (P 0.05); however, with the conservative TCA criteria it was (P 0.033). For the control analysis, patients showing visual field change during the initial follow-up with either criterion ( 1, 2, or 3 points) had significantly shorter survival times to subsequent visual field progression (P 0.030) compared with those with stable initial visual fields (Fig 3). For protocol A, these differences in mean survival times ranged from 2.9 to 3.0 years, and for protocol B, they ranged from 0.7 to 0.9 years. Rates of MD change during the subsequent follow-up in patients showing change and no change in the optic disc during the initial follow-up are shown in Figure 4. For all TCA criteria in protocols A and B, the mean MD slope was more negative (indicating a faster rate of visual field deterioration) in patients showing optic disc change compared with those showing no change. However, these differences failed to reach significance (P 0.100; Mann­Whitney test) for all criteria except with the moderate TCA criterion for protocol A (P 0.045). For the control analysis, the distributions of MD slopes during the subsequent follow-up in patients showing change and no change during the initial follow-up were widely overlapping (P 0.200; Fig 5) despite the fact that, with each criterion, the mean MD slope in patients with change during the initial follow-up was more negative.

Table 2. Number of Patients with Change for Each Criterion during the Initial Follow-up Period in the Test and Control Analyses*

Protocol A Analysis Test Liberal Moderate Conservative Control 1 point 2 points 3 points Change (%) 42 (52) 27 (33) 7 (9) 19 (23) 7 (9) 5 (6) No Change (%) 39 (48) 54 (67) 74 (91) 62 (77) 74 (91) 76 (94) Protocol B Change (%) 63 (78) 47 (58) 18 (22) 32 (40) 16 (20) 12 (15) No Change (%) 18 (22) 34 (42) 63 (78) 49 (60) 65 (80) 69 (85)

*Initial follow-up was with confocal scanning laser tomography in the test analysis and standard automated perimetry in the control analysis.

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Figure 2. Kaplan­Meier survival curves for subsequent visual field progression in protocols A and B in patients with and without optic disc change during the initial follow-up (test analysis). Three criteria for optic disc change with the Topographic Change Analysis, liberal, moderate, and conservative, were used. Table 2 provides the sample size for each group.

The positive and negative likelihood ratios of the 3 TCA criteria during the initial follow-up for visual field progression during the subsequent follow-up are shown in Table 3. These results indicate that the positive likelihood ratios were generally higher for the conservative TCA criteria and for protocol B when the initial follow-up period with CSLT was longer. The best (highest) positive likelihood ratio (3.02; protocol B, Table 3) indicates that a classification of optic disc change using the conservative TCA criterion was 3 times more likely to occur in patients showing subsequent visual field progression. This set of criteria also resulted in the best (lowest) negative likelihood ratio (0.53; protocol B, Table 3), indicating that absence of optic disc change with the conservative TCA criterion was only half as likely to occur in patients showing subsequent visual field progression. In all cases, the positive and negative likelihood ratios for the control analyses were respectively higher (2.44 ­5.25; Table 3) and generally lower (0.22­ 0.86; Table 3) than for the test analyses.

Discussion

New imaging devices for the optic disc have the potential to enhance the clinical care of glaucoma patients. Judging the merit of a new imaging technique in glaucoma typically relies on comparison with an accepted clinical methodology, or reference standard, such as conventional photography or clinical examination. For such comparisons, however, there are a priori assumptions that findings with any new technique should be detected, at the same time or in the

future, with the reference standard. Recently, we and others15,16,18,19 compared the performance of CSLT, specifically the TCA, with expert evaluation of conventional disc photographs and found a significant subset of patients who show optic disc changes with CSLT only,15,18 even with criteria thought to yield equivalent or higher specificity values than expert classification of disc photographs.15 Hence, requiring confirmation of the change with older reference standards introduces a bias and may limit the acceptance of new imaging devices. Baseline status of the optic disc1,23 and retinal nerve fiber layer24 ­26 in ocular hypertensive subjects is associated with subsequent visual field progression. However, to the best of our knowledge, the present study is the first published report on visual field progression after longitudinally detected change in the optic disc with CSLT in patients with established glaucoma. Because there are no accepted guidelines on the magnitude of optic disc change that constitutes clinical progression, we used 3 TCA criteria that cover a broad range of specificities.15 Similarly, we used different criteria for visual field change during the initial follow-up. For both a shorter (protocol A) or longer (protocol B) initial follow-up, patients with optic disc change with any criterion always had a shorter mean time to visual field progression during the subsequent follow-up compared with those without optic disc change. However, the differences in survival times were only significant when greater changes in

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Figure 3. Kaplan­Meier survival curves for subsequent visual field progression in protocols A and B in patients with and without visual field change during the initial follow-up (control analysis). Three criteria for visual field change during the initial follow-up, 1, 2, and 3 points with significant change, were used. Table 2 provides the sample size for each group.

the optic disc with a longer initial follow-up were required. This is most likely a function of the sample size; the absence of significance does not imply lack of a real, albeit relatively small, effect. In the control analysis, patients with visual field change during the initial follow-up always had a statistically shorter mean time to further progression during the subsequent follow-up. Patients with prior optic disc change had a more rapid rate of subsequent visual field progression; however, the distributions of MD slope in patients with and without optic disc change during the initial follow-up were widely overlapping. Similarly, patients with prior visual field change also always had worse subsequent mean rate of MD change; however, the rate differences between those with and without visual field change during the initial follow-up were not statistically different. The fact that the pointwise pattern deviation change criteria are better at predicting subsequent progression compared with rate of MD change is not surprising because the same analyses for the initial and subsequent follow-up were used. Rate of MD change reflects global change in the visual field and is a useful parameter for estimating the rate of visual field loss, particularly when frequent observations spanning many years are available; however, it is frequently uninfluenced by small, localized, and potentially clinically significant changes. Survival statistics are useful to compare group behavior; however, from an individual patient perspective, likelihood ratios provide a more practical index of the value of observ-

ing an optic disc change, irrespective of whether the mean survival times between groups are statistically different or not. Likelihood ratios can also be used to derive posttest (in this case, the presence or absence of optic disc change) probability of subsequent visual field progression after factoring in other clinical data that are used to estimate the pretest probability. The positive likelihood ratios increased with increasingly conservative TCA criteria, and also with a longer initial follow-up. In the control analysis, the likelihood of patients showing subsequent visual field progression was higher in patients with prior visual field change compared with prior optic disc change, and lower in patients with no prior field change compared with disc change. The results of this study have some practical implications for following patients with CSLT. Because the technique and statistical methods to analyze the data are relatively new, optimal criteria for follow-up have to be established with empirical data. Previously, we showed that the moderate and conservative TCA criteria, yielding a specificity of 94% and 97%, respectively, performed at least as well as classification of optic disc photographs by glaucoma specialists.15 In the present study, we showed that the conservative TCA criterion also yielded the best separation in survival time to subsequent visual field progression in patients with and without optic disc change during the initial follow-up. More important, this criterion also had the best positive and negative likelihood ratios for subsequent visual field progression. Hence, several lines of evidence support

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Figure 4. Box plots showing the distribution of rates of subsequent mean deviation (MD) change with standard automated perimetry in protocols A and B in patients with and without optic disc change with confocal scanning laser tomography (CSLT) during the initial follow-up (test analysis). Three criteria for optic disc change with the Topographic Change Analysis, liberal, moderate, and conservative, were used. Dot indicates mean; horizontal line inside box indicates median; box boundaries indicate 25th and 75th percentiles; and tails indicate 10th and 90th percentiles.

adoption of the moderate or conservative TCA criteria for clinical follow-up. The EMGT criterion for visual field progression, as used in this study, is incorporated into Humphrey Field Analyzer software and therefore widely available and used by clinicians. This criterion was recently shown to have good performance characteristics, including high specificity,20,27 which is important in clinical studies and trials.28,29 With 2 visual field examinations per year, the average time to detect visual field change using EMGT-like criteria is 4 to 5 years.30 For clinical studies and trials comparing treatment groups, depending on the differential treatment effect, the follow-up time required to show a group difference may be considerably longer. In many cases, this follow-up period may be unacceptably long because of cost, compliance, attrition, and other factors associated with extended followup. Employing more efficacious end points is likely to reduce the length of clinical studies and trials. We showed that, although prior visual field change is more predictive of subsequent visual field progression compared with prior optic disc change, the proportion of patients showing pro-

gression with the EMGT criterion during the initial follow-up was small (6% in protocol A and 15% in protocol B). Although this proportion can be increased using less conservative criteria ( 1 or 2 points), the number of patients with false-positive changes in the visual field will increase2 and reduce the efficacy of the end point. In contrast, for similar specificity, CSLT-defined changes yield a higher proportion of patients showing change. A key limitation of the present study is that its findings are likely to be dependent on the overall optic disc and visual field progression rates in our sample of patients. Previous studies show that average rates of MD change vary from 0 to 2.5 dB/yr,20,31­35 depending on disease severity, population sample, treatment, and length and frequency of follow-up. In the present study, the mean standard deviation rate of MD change in protocols A and B was modest: 0.21 0.45 and 0.22 0.45 dB/yr, respectively. The reason for this finding is not obvious; however, patients were participants in a longitudinal study in whom progression rates have been demonstrated to be lower than in nonstudy patients,36 perhaps because of higher treatment compliance.

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Figure 5. Box plots showing the distribution of rates of mean deviation (MD) change with standard automated perimetry (SAP) in protocols A and B in patients with and without visual field change during the initial follow-up (control analysis). Three criteria for visual field change during the initial follow-up, 1, 2, and 3 points with significant change, were used. Dot indicates mean; horizontal line inside box indicates median; box boundaries indicate 25th and 75th percentiles and tails indicate 10th and 90th percentiles.

Subsequent visual field progression may have been influenced by the nature of treatment decisions during the follow-up, which were at the discretion of the clinician, in addition to prior optic disc and visual field change. Visual field progression

rates would likely depend on the stage of the disease at baseline. For example, patients with more advanced damage may likely show further and faster visual field progression compared with those with less advanced damage.

Table 3. Positive and Negative Likelihood Ratios (LR) for Visual Field Progression during the Subsequent Follow-up*

Protocol A Analysis Test Liberal Moderate Conservative Control 1 point 2 points 3 points Positive LR 0.96 (0.57­1.60) 1.23 (0.62­2.43) 2.63 (0.65­10.67) 3.15 (1.51­6.55) 4.67 (1.15­18.97) 5.25 (0.95­29.05) Negative LR 1.05 (0.62­1.78) 0.90 (0.60­1.34) 0.89 (0.72­1.11) 0.59 (0.37­0.96) 0.82 (0.63­1.05) 0.86 (0.68­1.06) Positive LR 1.11 (0.80­1.54) 1.26 (0.76­2.09) 3.02 (1.36­6.70) 2.44 (1.58­3.76) 3.52 (1.55­8.04) 3.52 (1.23­10.09) Protocol B Negative LR 0.62 (0.10­4.00) 0.66 (0.20­2.19) 0.53 (0.22­1.25) 0.22 (0.04­1.36) 0.51 (0.22­1.21) 0.65 (0.34­1.24)

Values shown are LR and 95% confidence intervals. *Initial follow-up was with confocal scanning laser tomography in the test analysis and standard automated perimetry in the control analysis.

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14. Fayers T, Strouthidis NG, Garway-Heath DF. Monitoring glaucomatous progression using a novel Heidelberg retina tomograph event analysis. Ophthalmology 2007;114:1973­ 80. 15. Chauhan BC, Hutchison DM, Artes PH, et al. Optic disc progression in glaucoma: comparison of confocal scanning laser tomography to optic disc photographs in a prospective study. Invest Ophthalmol Vis Sci 2009;50:1682­91. 16. Chauhan BC, McCormick TA, Nicolela MT, LeBlanc RP. Optic disc and visual field changes in a prospective longitudinal study of patients with glaucoma: comparison of scanning laser tomography with conventional perimetry and optic disc photography. Arch Ophthalmol 2001;119:1492­9. 17. Ervin JC, Lemij HG, Mills RP, et al. Clinician change detection viewing longitudinal stereophotographs compared to confocal scanning laser tomography in the LSU Experimental Glaucoma (LEG) Study. Ophthalmology 2002;109:467­ 81. 18. Bowd C, Balasubramanian M, Weinreb RN, et al. Performance of confocal scanning laser tomograph Topographic Change Analysis (TCA) for assessing glaucomatous progression. Invest Ophthalmol Vis Sci 2009;50:691­701. 19. Kourkoutas D, Buys YM, Flanagan JG, et al. Comparison of glaucoma progression evaluated with Heidelberg retina tomograph II versus optic nerve head stereophotographs. Can J Ophthalmol 2007;42:82­ 8. 20. Artes PH, Nicolela MT, LeBlanc RP, Chauhan BC. Visual field progression in glaucoma: total versus pattern deviation analyses. Invest Ophthalmol Vis Sci 2005;46:4600 ­ 6. 21. Bengtsson B, Lindgren A, Heijl A, et al. Perimetric probability maps to separate change caused by glaucoma from that caused by cataract. Acta Ophthalmol Scand 1997;75:184 ­ 8. 22. Leske MC, Heijl A, Hyman L, Bengtsson B, Early Manifest Glaucoma Trial Group. Early Manifest Glaucoma Trial: design and baseline data. Ophthalmology 1999;106:2144 ­53. 23. Zangwill LM, Weinreb RN, Beiser JA, et al, Confocal Scanning Laser Ophthalmoscopy Ancillary Study to the Ocular Hypertension Treatment Study Group. Baseline topographic optic disc measurements are associated with the development of primary open-angle glaucoma: the Confocal Scanning Laser Ophthalmoscopy Ancillary Study to the Ocular Hypertension Treatment Study. Arch Ophthalmol 2005;123:1188 ­97. 24. Sommer A, Katz J, Quigley HA, et al. Clinically detectable nerve fiber atrophy precedes the onset of glaucomatous field loss. Arch Ophthalmol 1991;109:77­ 83. 25. Mohammadi K, Bowd C, Weinreb RN, et al. Retinal nerve fiber layer thickness measurements with scanning laser polarimetry predict glaucomatous visual field loss. Am J Ophthalmol 2004;138:592­ 601. 26. Lalezary M, Medeiros FA, Weinreb RN, et al. Baseline optical coherence tomography predicts the development of glaucomatous change in glaucoma suspects. Am J Ophthalmol 2006; 142:576 ­ 82. 27. Heijl A, Bengtsson B, Chauhan BC, et al. A comparison of visual field progression criteria of 3 major glaucoma trials in Early Manifest Glaucoma Trial patients. Ophthalmology 2008; 115:1557­ 65. 28. Schulzer M. Errors in the diagnosis of visual field progression in normal-tension glaucoma. Ophthalmology 1994; 101:1589 ­94. 29. Keltner JL, Johnson CA, Levine RA, et al, Ocular Hypertension Treatment Study Group. Normal visual field test results following glaucomatous visual field end points in the Ocular Hypertension Treatment Study. Arch Ophthalmol 2005;123: 1201­ 6. 30. Vesti E, Johnson CA, Chauhan BC. Comparison of different methods for detecting glaucomatous visual field progression. Invest Ophthalmol Vis Sci 2003;44:3873­9.

In summary, the present study shows that patients with subsequent field progression were up to 3 times more likely to have prior disc change during the initial follow-up compared with those without field progression. The mean time to visual field progression is also shorter in these patients. In comparison, patients with subsequent visual field progression are even more likely to have prior visual field change. The higher number of patients showing TCA change at comparable levels of specificity suggest that optic disc end points may be an alternative means to gauge future progression in glaucoma.

References

1. Johnson CA, Sample PA, Zangwill LM, et al. Structure and function evaluation (SAFE): II. Comparison of optic disk and visual field characteristics. Am J Ophthalmol 2003;135:148 ­54. 2. Artes PH, Chauhan BC. Longitudinal changes in the visual field and optic disc in glaucoma. Prog Retin Eye Res 2005; 24:333­54. 3. Strouthidis NG, Scott A, Peter NM, Garway-Heath DF. Optic disc and visual field progression in ocular hypertensive subjects: detection rates, specificity, and agreement. Invest Ophthalmol Vis Sci 2006;47:2904 ­10. 4. Collaborative Normal-Tension Glaucoma Study Group. Comparison of glaucomatous progression between untreated patients with normal-tension glaucoma and patients with therapeutically reduced intraocular pressures. Am J Ophthalmol 1998;126:487­97. 5. Heijl A, Leske MC, Bengtsson B, et al, Early Manifest Glaucoma Trial Group. Reduction of intraocular pressure and glaucoma progression: results from the Early Manifest Glaucoma Trial. Arch Ophthalmol 2002;120:1268 ­79. 6. Kass MA, Heuer DK, Higginbotham EJ, et al, Ocular Hypertension Treatment Study Group. The Ocular Hypertension Treatment Study: a randomized trial determines that topical ocular hypotensive medication delays or prevents the onset of primary open-angle glaucoma. Arch Ophthalmol 2002;120:701­13. 7. Zinser G, Wijnaendts-van-Resandt RW, Dreher AW, et al. Confocal laser tomographic scanning of the eye. In: Wampler, JE, ed. New Methods in Microscopy and Low Light Imaging. Bellingham, WA: SPIE; 1989:337­ 44. Proceedings/SPIE 1161. 8. Mikelberg FS, Parfitt CM, Swindale NV, et al. Ability of the Heidelberg retina tomograph to detect early glaucomatous visual field loss. J Glaucoma 1995;4:242­7. 9. Bathija R, Zangwill L, Berry CC, et al. Detection of early glaucomatous structural damage with confocal scanning laser tomography. J Glaucoma 1998;7:121­7. 10. Wollstein G, Garway-Heath DF, Hitchings RA. Identification of early glaucoma cases with the scanning laser ophthalmoscope. Ophthalmology 1998;105:1557­ 63. 11. Swindale NV, Stjepanovic G, Chin A, Mikelberg FS. Automated analysis of normal and glaucomatous optic nerve head topography images. Invest Ophthalmol Vis Sci 2000;41: 1730 ­ 42. 12. Chauhan BC, Blanchard JW, Hamilton DC, LeBlanc RP. Technique for detecting serial topographic changes in the optic disc and peripapillary retina using scanning laser tomography. Invest Ophthalmol Vis Sci 2000;41:775­ 82. 13. Patterson AJ, Garway-Heath DF, Strouthidis NG, Crabb DP. A new statistical approach for quantifying change in series of retinal and optic nerve head topography images. Invest Ophthalmol Vis Sci 2005;46:1659 ­ 67.

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31. Smith SD, Katz J, Quigley HA. Analysis of progressive change in automated visual fields in glaucoma. Invest Ophthalmol Vis Sci 1996;37:1419 ­28. 32. Collaborative Normal-Tension Glaucoma Study Group. Natural history of normal-tension glaucoma. Ophthalmology 2001;108:247­53. 33. Shigeeda T, Tomidokoro A, Araie M, et al. Long-term follow-up of visual field progression after trabeculectomy in progressive normal-tension glaucoma. Ophthalmology 2002; 109:766 ­70. 34. Lee YH, Kim CS, Hong SP. Rate of visual field progression in primary open-angle glaucoma and primary angle-closure glaucoma. Korean J Ophthalmol 2004;18:106 ­15. 35. Schwartz B, Takamoto T, Martin J. Increased rate of visual field loss associated with larger initial visual field threshold values on follow-up of open-angle glaucoma. J Glaucoma 2004;13:120 ­9. 36. Henson DB, Shambhu S. Relative risk of progressive glaucomatous visual field loss in patients enrolled and not enrolled in a prospective longitudinal study. Arch Ophthalmol 2006;124:1405­8.

Footnotes

Originally received: January 17, 2009. Final revision: April 10, 2009. Accepted: April 15, 2009. Available online: June 4, 2009. Supported by Grant MOP11357 from the Canadian Institutes of Health Research (BCC). Manuscript no. 2009-75. Correspondence: Balwantray C. Chauhan, PhD, Department of Ophthalmology and Visual Sciences, Dalhousie University, 1276 South Park Street, 2W Victoria, Halifax, NS, Canada B3H 2Y9. E-mail: [email protected]

Department of Ophthalmology and Visual Sciences, Dalhousie University, Halifax, Nova Scotia, Canada.

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